Conservation – Page 26 – Shark Research & Conservation Program (SRC)

Fishy Behavior: The Effect of Local Fishing on Coral Reef Fish Behavior

March 31, 2015/0 Comments/in Conservation, Ocean News /by aanstett

By Dani Ferraro, RJD student

In the Indo-Pacific, coral reef fish have encountered behavioral changes due to increasing local fishing efforts. The rise of commercial fishing and local fishing have caused a change in species composition, abundance, and behavior of species inside protected areas. In an experiment done by Fraser A. Januchowski-Hartley et al, two target species were monitored in both marine reserves (Chagos) as well as well-fished areas in the Philippines. They measured the correlation between fishing pressure, fish size, habitat complexity and life-history stage against the fish flight initiation distance (FID). This yielded a conclusion that fish FID increased with outside fishing pressure in both locations, implying that commercial fishing affects adjacent areas as well.

When studying the consequences of fishing upon coral reef fish populations, it’s important to consider both the long-term and short-term effects upon the ecosystem. Both commercial fishing and local fisheries affect the biomass, abundance, structure and function of fish populations, as well as the biodiversity (Estes et al., 2011). Increased fishing rates paired with species-specific targeting results in a devastating overfishing problem, especially when considering coral reef species. These species are also targeted indirectly with the release of keystone invasive species, such as urchins and lionfish. A result upon coral reef fish behavior is demonstrated through “wary” behaviors, such as remaining closer to shelter or faster reaction time to predators.

Although marine reserves offer higher protection levels for species, allowing them to rebuild their stocks, a perhaps more telling result is the decrease in flight behaviors of coral reef fishes. Those fish that have spent a greater period of time in marine protected areas show less wary behavior than those under the constant threat of fishing. This more confident fish behavior bleeds over the lines of marine protected areas into the adjacent zones. However, this also lends to the idea that the pressure of commercial fishing could impact ecosystems protected by marine reserves. “Fishing the line” refers to the reduction in both abundance and biodiversity along the boundary of marine protected areas due to increased fishing efforts. The flight initiation distance (FID) measures how close an observer or predator can get to an animal before it flees. This experiment analyzes the influences of anthropogenic and environmental factors on an ecosystem and the range of fish behaviors with proximity to fishing pressure in both marine protected areas and high pressure areas.

The Chagos Archipelago is the world’s largest marine reserve in the world, with an area of 250,000 square miles. Image Source: Wikimedia Commons

In the experiment by Januchowski, there was a positive correlation between fish size and increases in FID found in fished areas. In the protected areas in Chagos, Januchowski iterated that there was a significantly lower FID than those of other locations. However, while the original intent was to study the relationship between fishing pressure and fish behavior, measured in FID. However, they found that the two were related within protected marine reserves embedded in “fished seascapes.” Coral reef fish within these areas displayed high levels of wary behavior around humans and predators with a parallel increase in fishing pressure outside of these zones. This finding has implications for the future roles of marine reserves for fish species conservation, especially in regard to distribution of fishing efforts.

References

Estes, J.A. et al., 2011. Trophic downgrading of planet Earth. Science 333, 301–306.

http://dx.doi.org/10.1126/science.1205106

Januchowski-Hartley, Fraser A, Nicholas A.J. Graham, Joshua E. Cinner, and Garry R. Russ. “Local Fishing Influences Coral Reef Fish Behavior inside Protected Areas of the Indo-Pacific.” Biological Conservation 182 (2014): 8-12. Print.

The consequences of harmful algal blooms and their production of paralytic shellfish toxins

March 30, 2015/0 Comments/in Conservation, Ocean News /by aanstett

by Laurel Zaima, RJD intern

Harmful algal blooms (HABs) are a large concern for many who live on the coasts. People are told to avoid eating local seafood and contact with the contaminated water. However, the consequences of HABs extend much further than many people realize. HABs are associated with high fish mortality, which disturbs the entire effected marine and coastal ecosystem. During HABs, there are high cell densities of toxin-producing phytoplankton species. These phytoplankton produce a paralytic shellfish toxin (PST) and they are easily ingested by planktivorous fish or filter-feeding organisms. Once the toxin has entered the food web, PSTs can impact multiple trophic levels. (Picture 1: An expansive harmful algal bloom is prominently seen off the coast of Gotland, a Swedish Island in the Baltic Sea.) PSTs are a worldwide concern because they are concentrated and abundant near the coasts and have detrimental affects on aquaculture, fisheries, human health, industries, and economies. In the scientific paper, Impact and effects of paralytic shellfish poisoning toxins derived from harmful algal blooms to marine fish, Costa (2014) assess the fish contamination, fish mortality, and the ecosystem-wide implications of these toxins in order to better understand and help to better manage the damaging effects of PSTs.

Paralytic shellfish toxins are produced in the marine environment by nine dinoflagellate species. Each of the PSTs have slight differences in the structure of their functional groups, which results in different toxicity levels. (Picture 2: The chemical structure of the paralytic shellfish toxins (PSTs)). Fish that are exposed to PST exhibit irregular swim and motor behaviors, such as swimming on their sides or upside down and gaping at the surface. With extensive exposure to PSTs, the toxin causes subsequent paralysis in the muscles. Therefore, PSTs prevent fish from effectively foraging or avoiding predators. Ultimately, the most common result of the toxicity is death.

Fish mortality associated with PSTs have been reported worldwide. Fish species involved in the toxic episodes include planktivorous fish that feed directly on the toxic algae, planktivorous fish that ingested contaminated zooplankton that have fed on the toxic algae, predators species that have fed on the contaminated fish or shellfish, and fish that are artificially fed but were directly exposed to the toxic algae. The PSTs that are produced by harmful algal blooms can modify the predator-prey interactions that can lead to a cascading affect on the coastal food web and community structures in the marine systems. PSTs hold consequences for organisms at various trophic levels from the ability to initiate a top-down or bottom-up trophic cascade. Humans have also been contaminated by PSTs in various countries from ingesting toxic fish. After people were directly affected by PSTs, action towards algal management was implemented in several countries. Countries in South-East Asia have employed laws that enforce the identification and count of the toxic phytoplankton in seawater, a measure of the toxicity in the shellfish, and a constant monitoring of the marine toxins in planktivorous fish before declaring the local fish acceptable for consumption.

Harmful algal bloom from Costa 2014

The neurotoxic paralytic shellfish toxins have negative impacts on the fish populations and any associated marine and terrestrial organisms. PSTs have an apparent significance on the function of the ecosystem, and therefore, there is an increasing importance in understanding, managing and monitoring the issue. In terms of ecosystem-based management, it is imperative that fish are properly characterized by their levels of PST exposure from direct consumption and through potential intermediate vectors in order to keep seafood consumers safe from the toxins.

Impact and effects of paralytic shellfish poisoning toxins derived from harmful algal blooms to marine fish
P Reis Costa – Fish and Fisheries, 2014

The Truth Behind Catch-and-Release of Atlantic cod

March 27, 2015/0 Comments/in Conservation, Ocean News /by aanstett

By Jessica Wingar, RJD Intern

With decreasing fish stocks, there has been an increase fishing regulations. One of these categories of fishing is recreational fishing, which includes catch and release fishing. In catch and release fishing, the fish is released back into the ocean after being reeled in. Despite the fact that this practice puts the fish back in its habitat, the process can have detrimental effects on the fish. An example of one of these disadvantages is the damage caused by the hook; the hook can become lodged in the body cavity of the fish and cause damage that could cause mortality. There are numerous different studies that can be conducted to look at post release in fish, but telemetry studies are becoming more numerous because they allow the fish species to be studied in its habitat and provides effective data. In this method, tags are surgically inserted into the fish and the fish are released back into the environment. In order to differentiate between the effects of surgery and release, the fish are captured again after a surgery recovery period to find out the affects of the release. Since the fish are captured again, it is critical that the species studied does not live in a large area. This study method was used to examine Atlantic cod in Norway.

Atlantic cod were chosen as the study species because they have a known small range that they inhabit. In addition, they are a commonly released fish. In this study, the researchers wanted to study what the post release effects would be of the fish coming from depth. The reason why the researchers wanted to study the effects of depth is because Atlantic cod have a closed physoclistous swim bladder, which means that their swim bladder can expand if they are pulled from a depth, such as what occurs when they are reeled in. In this study, eighty cod were surgically implanted with acoustic transmitters and the fish were tagged. Ultrasonic receivers were placed in the study area to determine how the fish were moving up and down the water column. These fish were released, and after a recovery time, nine were recaptured in order to determine the affects on vertical migration after release.

The study area in Norway

This study demonstrated that there was not a significant difference in vertical migration after the release of all eighty cod. In addition, there was not a significant difference in vertical migration after the release of the nine cod caught again after the surgery. Although the results are not statistically significant, the researchers found that some small-scale changes could occur immediately after release, but that these changes are not permanent. However, these small-scale changes could have implications for successful mating and other behaviors. The reason behind why some cod were affected, while others were not could lie in the fact that physiology differs between each individual. In conclusion, with proper fishing equipment and practices, catch and release fishing has few detrimental effects on Atlantic cod in Norway.

Depth results from the initial eighty cod and the recaptured and released cod

Studies like this one are increasingly critical to the conservation of fish species, such as Atlantic cod. They are important because they provide a platform to promote safe fishing practices and methods, such as using a circle hook, for recreational fishermen. If more fishermen who fish for sport, used safe fishing techniques, then the cod fished will not be as affected by catch and release fishing.

Reference

Ferter, K., Hartmann, K., Kleiven, A.R., Moland, E., and Esben Moland Olsen. “Catch-and-release of Atlantic cod (Gadus morhua): post-release behavior of acoustically pretagged fish in a natural marine environment.” Canadian Journal of Fisheries and Aquatic Sciences 72 (2015):1-10.

Threats to Sea Otters

March 23, 2015/0 Comments/in Conservation, Ocean News /by aanstett

by Daniela Escontrela, RJD intern

Sea otters are a very charismatic species due to their very cute and cuddly appearance; however, sea otters are quite interesting animals for many reasons. For one sea otters lack a blubber layer like many other marine mammals. To make up for this, they have the thickets fur of any animal coming in at one million hairs per square inch, 800 million total (compare that to humans who have a mere 100,000 hairs on their entire heads) (Cohn 1998). Otters are also the only marine animal known to use tools. They place a rock on its belly while they float on their back and strike mussels and clams against them to open them. They will consume one quarter of their body weight in food and their high metabolic system quickly turns that food into heat energy. Sea otters are slow reproducers, having one pup every two years (Waldichuk 1990). Additionally, sea otters were one of the last marine mammals to adapt to life in the ocean and they are the second smallest marine mammal (Cohn 1998). Sea otters spend most of their time at sea; in fact when sleeping they will wrap themselves in kelp to keep from drifting away with the current (Waldichuk 1990).

Figure 1. A sea otter at the Monterrey Bay Aquarium laying on its back, a characteristic pose of this animal (Cohn 1998).

However, as cute and charismatic as these animals are, they have suffered great tragedy. Sea otters in North America were first discovered in 1742 by Vitus Bering from Russia who got shipwrecked in the Bring Sea (Waldichuk 1990). At the time, otters ranged from Japan and the Kamchatka Peninsula across the Commander and Aleutian islands to Alaska and down the west coast of North America to Baja California. The shipwrecked survivors first used the otters for food but soon discovered how valuable the coats could be. When word got back to Russia, people from all over the world would make their way to the west coast of North America to hunt the animals for their fur (Cohn 1998). These animals were hunted all throughout the 18th and 19th century and estimates are that 400,000 were killed in that time. By the 1900s, only a few dozen remained in California with a few handfuls in other regions (Lafferty and Tinker 2014). In 1911 the animals were saved from extinction when Canada, Russia, Japan and the USA signed a treaty, called the International Fur Treaty, to stop killing them, at which point only 1000-2000 remained in the wild (Waldichuk 1990). In addition, the sea otters were listed as “threatened” under the endangered species act, the marine mammal protection act listed them as depleted and California as a “fully protected mammal”; they are also protected under Russian law (Cohn 1998).

In the recovery process sea otters have been relocated from areas where they are abundant to areas where they are depleted. In the past couple of decades numbers have increased to ~150,000 in Alaska and the Aleutian islands, 17,000-18,000 in Russia and northern Japan, 1000 in British Columbia, 2000 in California and 500 in Washington (Cohn 1998). Even though it seems sea otters are out of danger that is far from the truth. Although they are no longer exploited for their fur, there exist other threats. For one, sea otters are highly susceptible to oil spills. Sea otters spend a lot of time grooming their fur and as such they are highly vulnerable to ingestion if coated in oil. When the Exxon Valdez oil spill occurred in the Prince William Sound in Alaska, 42 million liters of oil were released into the water killing at least 450 sea otters. Many suffered from liver damage due to ingestion of oil during grooming. In addition, the fur is also susceptible to oil as the underfur layer, which usually stays dry, loses the insulation quality and animals end up dying of pneumonia. Although a large oil spill hasn’t occurred in California, many conservationists want the introduction of sea otters into southern California, where they were once abundant, in the case of a spill (Waldichuk 1990). However, expansion into southern California has been sporadic. Sea otters prefer to stay near shore and at the moment, sea otter abundance in central California may be at its carrying capacity limited by food and shelter. If southern California can hold the same density of otters as central California then sea otter populations could rise to 16,000; clearly range expansion is key to further population recovery. In an effort to direct an expansion of sea otters while minimizing competition with fishermen, US Fish and Wildlife created a “no-otter” management zone south of Point Conception (which divides central from southern California). For many years, if otters were found to the south of this they would be relocated to central California. However, in 1998 a group of 93 males was seen south of Point Conception, a group too large to relocate. Since then patterns of migration have been observed for the otters. Males will travel south from winter to spring in search of resources then return to the center ranger after females wean their pups and come into estrous. These groups of non-territorial males at the range margins colonize adjacent open habitat to exploit abundant resources, often in response to increasing prey competition the previous neighboring habitat they occupied. If these males stay in this territory for 5 to 10 years, other females and pups will begin to arrive. At this point there is a demographic transition from male colony to mix sexed groups. Males will then establish territories which forces non-territorial males to move again to new territory and to start the cycle again. This cycle makes growth and expansion slow and intermittent. In December 2012 US Fish and Wildlife Service determined the California translocation program a failure and ended it, halting enforcement of the “no-otter” management zone (Lafferty and Tinker 2014). If this pattern of southern expansion continues, sea otters could become more resilient to oil spills if they were to occur since the population would be spread out rather than clustered in central California.

Figure 2. Map of sea otter counts (red circles) and maximum kelp coverage south of Point Conception (Lafferty and Tinker 2014).

This migration of sea otters towards southern California is a step in the right direction; however, other threats still abound especially in California were growth rates lag behind at 5% per year, compared to 15-20% per year for Washington. This slow growth rate may be due to the high mortality rate of pups (40%) which is far higher than in other places. Previously, many males were dying from gill nets since males rest and feed further from shore where they are more susceptible to encounter these nets; luckily gillnets have been band. Natural threats include predation from sharks, especially in the North, and from killer whales. Another major threat is a parasitic worm that hits juveniles and pups; this worm normally infests seabirds. A veterinary pathologist that examined 250 corpses found that 40% had died from this infectious disease. Sea otters are also susceptible to San Joaquin valley fever, a fungal disease usually seen in people living in arid areas. It is proposed that the disease finds its way to sea through airborne dust (Cohn 1998). If this wasn’t enough, another disease was discovered to also cause mortality in otters called Toxoplasma gondii. This single celled protozoan is pathogenic and causes protozoal encephalitis in otters. This is a deadly brain infection that causes tremors in the front legs and loss of muscle action. This prevents the animal from diving for food and grooming (a healthy sea otter spends one third of its day grooming). T. gondii comes from cats who excrete the protozoan’s eggs in their feces. The eggs can survive up to 18 months and due to rain off it makes its way to the ocean. As of 2003, out of 1000 dead sea otters that had washed up along the California coastline, 62% of them had died from the Protozoan infection (McLaughlin 2003).

The threats abound to sea otters who happen to be a keystone species. A keystone species is a plant or animal that plays a crucial role in the way an ecosystem functions. Without a keystone species, the ecosystem would be dramatically different or cease to exist altogether. Sea otters prefer coastal marine habitats dominated by kelp stands where they can find one of their staple food items, sea urchins. Heavy overgrazing by sea urchins on kelp forests can deplete them. However, if sea otters are present they can keep urchin levels low which prevents overgrazing (William 1988). In a study after the Exxon Valdez oil spill it was found that oiled areas where there were few sea otters had 1.52 urchins per 100 square meters versus 0.17 urchins per 100 square meters in non-oiled areas were otters were more abundant. These areas with higher densities of urchins experienced overgrazing and depletion of kelp forests. In fact some scientists believe that North American kelp evolved with otters. Kelp in Australian waters produce toxins to ward off urchins whereas kelp in North America do not produce this toxin since it did not need chemical defenses due to the presence of otters. It is important to keep sea otters around as they can help modify environments such as kelp forests which provide shelter and food for countless fish, shellfish, urchins and marine mammals and birds (Cohn 1998). It is of extreme importance that more research go into sea otter conservation to study things such as the diseases that are killing them and to come up with recovery plans in the case of an oil spill; arguably these are two of the biggest threats they face that we must confront in the near future if we don’t want to drive them to extinction.

Works Cited:
Jeffrey, P Cohn. “Understanding Sea Otters.” BioScience 48.3 (1998): 151-155.
Lafferty, Kevin D and Tim M Tinker. “Sea otters are recolonizing southern California in fits and starts.” Ecosphere 5.5 (2014): 1-11.
McLaughlin, Sabrina. “The Otter Limits.” Current Science 88.14 (2003): 4-5.
Waldichuk, M. “Sea Otters and Oil Pollution.” Marine Pollution Bulletin 21.1 (1990): 10-15.
William, Booth. “The Otter-Urchin-Kelp Scenario.” Science 241.4862 (1988): 157.

Current threats to coastal seagrass ecosystems

March 18, 2015/0 Comments/in Conservation, Ocean News /by aanstett

By Hanover Matz, RJD Intern

If asked what marine ecosystems are currently most at risk, many people would probably identify coral reefs and mangrove forests. Climate change, sea level rise, and habitat degradation are all terms that come to mind when addressing the decline of corals and mangroves worldwide. However, equally important and at risk are seagrass ecosystems. Seagrasses are marine flowering plants that form ecologically important coastal habitats in tropic and temperate oceans, playing a key role in unison with coral reefs and mangroves (Short et al., 2011). These three habitats exchange nutrients and organic matter, and seagrasses provide important habitat for many species of marine fauna and juvenile fish (van Tussenbroek et al., 2014). Endangered megafauna such as manatees, dugongs, and sea turtles graze on seagrass beds. In addition to supporting marine biodiversity, seagrass beds provide many benefits to human society. They support fisheries and provide livelihoods for millions of people in coastal communities (Short et al., 2011). Seagrass beds also maintain water quality and reduce turbidity through sediment deposition. By acting as nurseries for many economically important fish species such as snapper and grouper, they help support both tourism and fisheries (Lirman et al., 2014). Due to increasing anthropogenic threats to seagrass ecosystems, we are in danger of losing these important benefits.

A green sea turtle grazes on seagrass, an important food source for this endangered species. Photo courtesy of P. Lindgren via Wikimedia Commons

In order to implement conservation measures, the current status of seagrass species must be established. An evaluation of the world’s seagrass species by Short et al. (2011) utilized criterion set forth by the International Union for the Conservation of Nature (IUCN) to determine the risk of extinction for each seagrass species. The IUCN uses extinction risk theory and data on population reduction and geographic range to determine the conservation status of a species, ranked as Extinct, Critically Endangered, Endangered, Vulnerable, Near Threatened, Least Concern or Data Deficient. Seagrass experts used these criteria along with data on 72 species of seagrass to determine the vulnerability of each species. Based on the results of Short et al., fifteen species of seagrass were found to be threatened (Endangered/Vulnerable) or Near Threatened, with three considered Endangered. While forty-eight seagrass species were considered Least Concern, twenty-two were considered to have declining populations. This evaluation shows that while only a few seagrass species may be currently threatened with extinction, if population trends continue, many more species may be facing significant reductions in geographic range in the future. Figure 2 below shows the number of seagrass species with declining populations across the globe. The region with the highest number of declining species, the coasts of China, Japan, and Korea, corresponds with areas of high human development.

Global distribution of declining species of seagrass (Short et al., 2011)

Along with the IUCN Red List evaluation, the Caribbean Coastal Marine Productivity (CARICOMP) program has monitored seagrass communities in the Caribbean from 1992-2007 for changes in biomass and productivity. With data taken from 52 monitoring stations across the Caribbean, van Tussenbroek et al. (2014) assessed the impact of human activities on seagrass habitats. Forty-three percent of the seagrass communities at thirty-five of the long-term monitoring stations showed changes in biomass and productivity associated with environmental degradation. The authors indicated increased terrestrial run-off (sewage, fertilizer, and/or sediments) as the major anthropogenic influence on seagrasses in the Caribbean. Figure 3 shows the distribution of human impacted monitoring stations across the Caribbean. Like the IUCN Red List evaluation by Short et al., this study shows that we are just beginning to understand the effects human activities have had on seagrass habitats, and that these impacts will likely increase in the near future.

Distribution of seagrass community monitoring stations in the Caribbean, indicating communities potentially altered by environmental degradation (van Tussenbroek et al., 2014)

If seagrasses are on the decline, what is that primary cause of this decline? By combining the knowledge of several seagrass experts, Grech et al. (2012) identified many of the major threats to seagrass communities. Of the threats assessed, industrial and agricultural run-off, coastal infrastructure development, and dredging were determined to have the greatests impacts on seagrasses globally. These anthropogenic activities disturb seagrasses by increasing water turbidity and physically damaging seagrass habitat. Aquaculture development, trawling, and boat damage can also harm coastal seagrass communities. In addition to these direct human activities, climate change, sea level rise, and increasing severity of tropical storms were seen as potential risks for seagrasses (Grech et al., 2012). An example of how human activity can alter seagrass communities in South Florida was demonstrated by a study conducted in western Biscayne Bay (Lirman et al., 2014). Lirman et al. found that the proximity of the major metropolitan center, Miami, and changes in hydrology due to efforts to restore the Everglades have caused shifts in coastal salinity. These changes in turn have altered the composition of seagrass communities composed primarily of Thalassia, Halodule, and Syringodium seagrass species. Changes in salinity and nutrient availability may possibly cause the decline of seagrass dominated communities in exchange for macroalgae domianted communities. Once again, the association of human development can have serious consequences for coastal ecosystems.

In the face of all of these threats, what can be done to protect and conserve seagrasses? In an evaluation of coastal resource degradation, Wilkinson and Salvat (2012) assessed possible management solutions to help protect coral reefs, mangroves, and seagrasses. These resourcees have often been described as “commons”, open for access to anyone, but in reality these resources generally fall under the control of local coastal communities. In order to manage seagrasses, effective policies must be implemented at the local level. However, there is a disconnect between the regions of conservation research (developed nations), and the primary regions of seagrass habitat (developing nations). If seagrasses are to be protected through the use of management and Marine Protected Areas (MPAs), there must be greater cooperation between governments, policy makers, and scientists both at the national and international level (Wilkinson and Salvat, 2012). The global status of seagrass species and the current threats facing them have been established. While more research will certainly be beneficial, we need to focus on reducing the impacts of human activities. The best possible management effort will take into account all users of seagrass ecosystems, so that they can be used but not overexploited for future generations.

References

Grech, A., K. Chartrand-Miller, P. Erftemeijer, M. Fonseca, L. McKenzie, M. Rasheed, H. Taylor and R. Coles (2012). “A comparison of threats, vulnerabilities and management approaches in global seagrass bioregions.” Environmental Research Letters 7(2): 024006.
Lirman, D., T. Thyberg, R. Santos, S. Schopmeyer, C. Drury, L. Collado-Vides, S. Bellmund and J. Serafy (2014). “SAV Communities of Western Biscayne Bay, Miami, Florida, USA: Human and Natural Drivers of Seagrass and Macroalgae Abundance and Distribution Along a Continuous Shoreline.” Estuaries and Coasts 37(5): 1243-1255.
Short, F. T., B. Polidoro, S. R. Livingstone, K. E. Carpenter, S. Bandeira, J. S. Bujang, H. P. Calumpong, T. J. B. Carruthers, R. G. Coles, W. C. Dennison, P. L. A. Erftemeijer, M. D. Fortes, A. S. Freeman, T. G. Jagtap, A. H. M. Kamal, G. A. Kendrick, W. Judson Kenworthy, Y. A. La Nafie, I. M. Nasution, R. J. Orth, A. Prathep, J. C. Sanciangco, B. v. Tussenbroek, S. G. Vergara, M. Waycott and J. C. Zieman (2011). “Extinction risk assessment of the world’s seagrass species.” Biological Conservation.
van Tussenbroek, B. I., J. Cortes, R. Collin, A. C. Fonseca, P. M. Gayle, H. M. Guzman, G. E. Jacome, R. Juman, K. H. Koltes, H. A. Oxenford, A. Rodriguez-Ramirez, J. Samper-Villarreal, S. R. Smith, J. J. Tschirky and E. Weil (2014). “Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse.” PLoS One 9(3): e90600.
Wilkinson, C. and B. Salvat (2012). “Coastal resource degradation in the tropics: does the tragedy of the commons apply for coral reefs, mangrove forests and seagrass beds.” Mar Pollut Bull 64(6): 1096-1105.

The aquarium hobby’s impact on freshwater fish conservation

March 16, 2015/0 Comments/in Conservation, Ocean News /by aanstett

by Jacob Jerome, RJD student

From small bowls that house beta fish, to extensive aquariums with hundreds of individuals, fish are found in homes around the world. Through this hobby, people have the opportunity to experience the world of fish in a way that was never possible before. But there can be drawbacks to the aquarium hobby that concern researchers in regards to freshwater fish conservation. While acknowledging these problems, Maceda-Veiga et al aim to change the perception of hobbyists and show their potential to help conserve the fish that they love.

The major drawbacks of the aquarium hobby are the overharvesting of species and the introduction of invasive species to ecosystems around the world. Efforts have been put in place by scientists and conservationists to alleviate these issues but because of the huge popularity of the aquarium hobby, there is no short term solution. Cooperation between both aquarists and scientists is needed in order to reduce the effects of these problems and help promote freshwater fish conservation. To help push this cooperation, Maceda-Veiga et al point out some misconceptions of hobbyists and ways in which serious aquarium hobbyists and their organizations can aid scientists in their efforts.

: Illustrations of different understandings and philosophies about the aquarium hobby. (Maceda-Veiga et al

While it is perceived that hobbyists are doing nothing to help fix these two major drawbacks, as a whole, there has been progress towards minimizing them. For example, 90% of freshwater aquarium species are raised domestically and are not harvested from the wild. Interestingly, Maceda-Veiga et al found that aquarium keepers actually prefer these domestically raised fish due to their better appearances than the wild caught ones. To help reduce the introduction of invasive species, several aquarium hobbyist associations have published information in their magazines and websites to help educate aquarium keepers. In addition, many associations will accept fish returns so fish are not released into the wild.

Serious aquarium hobbyists can aid scientists in freshwater fish conservation as well. Hobbyists often contribute to the development of basic knowledge of species through their observations and success as aquarists. While the validity of these published findings in aquarium magazines and websites can be uncertain, they can reveal information to researchers to help them as they study a species. Hobbyists can also help to save species from extinction. Populations of fish kept in aquariums around the world can provide a gene bank to prevent the total extinction of a species or to help reintroduction programs. For example, the crescent zoe and the golden skiffia, two species extinct or nearly extinct in the wild, have been kept alive by dedicated hobbyists for over twenty five years.

An adult male (below) and female crescent zoe.

While the aquarium hobby has its drawbacks, it also has a potential to help conservation efforts. With more collaboration between enthusiast and scientists, much can be gained in the area of freshwater fish conservation. Working together, the negative aspects of aquarium keeping can be diminished while promoting conservation and helping to protect the fish that both groups love.

Reference:

Maceda-Veiga, A., Dominguez-Dominguez, O., Escribano-Alacid, J., Lyons, J. (2014). “The aquarium hobby: can sinners become saints in freshwater fish conservation?” Fish and Fisheries doi: 10.1111/faf.12097

What 19th century stories can tell us about modern fish stocks

March 13, 2015/0 Comments/in Conservation, Ocean News /by aanstett

By Stephen Cain, RJD Intern

Shifting baselines, a term introduced by Daniel Pauly in 1995, occur when successive generations view contemporary environmental conditions as the baseline to measure future change against. The problem with this sort of bounded rationality is that it fails to account for long-term historic trends, and risks myopic decision-making in the greater context. This has been the error of monitoring global fish stocks. In 2001, Jeremy Jackson and several researchers suggested that humans began interacting in coastal ecosystems 10,000 years ago. However, developed nations only recently implemented monitoring fish stocks after the Second World War, with reliable reporting covering the last 40 years. Some of the more robust reporting involve economically important species, and often provide sparse information on non-target species. In the end, our understanding of virginal abundance, and the overall depletion of it, is piecemeal.

Enter Ruth Thurstan and researchers from The University of Queensland, in a partnership with the Australian government. In their recent study on the iconic Australian Snapper (Pagrus Auratus), Thurstan and her team examined two times sets of data: from 1879 to 1939 (development of the fishery), and 1940 to 2003. They devised a novel approach that has extended the baseline for the fishery back to the late 19^th century. They argue that catch rates based on current fishing effort depict a fishery in decline since 1879. By their estimates, Snapper have declined by as much as 90%. Stable catch rates over time may have masked local declines as the fishery expanded its grounds and better technology became available.

Snapper are a species of bony fish that inhabit the rocky reefs of Eastern, Southern, and Western Australia. They range seas from New Zealand to Japan, and can live up to 30 years. In Eastern and Southern Australia, where the team collected data, the recreational Snapper fishery is estimated to be as much as 3 times larger than the commercial fishery. Because the relationship between Australians and Snapper goes back at least 130 years, the social and cultural context matters. According to Thurstan et al., while current gear, size, and allowable catch restrictions are in place, any future efforts to preserve the stock must exercise an understanding of the social ties to Snapper.

Historical ecology, or the study of ecosystems over time, is a discipline that has helped to address some of the issues of shifting baselines. As Thurstan et al. discuss, the trouble with examining their historical data, such as old newspapers, popular literature, and early scientific surveys, is that that information was incomplete, difficult to quantify, or suffered from reporting bias. On the other hand, they suggested that early data yielded qualitative insights that shaped assumptions about fishing effort over a longer time scale.

By piecing missing data together using relevant multiple imputation, the team generated catch rate data (derived from the number of fish, number of fishers, and time spent) that did not statistically differ from complete sources that allowed for cross-reference. The results were encouraging. By using narrative accounts of fish abundance, gear types, and information on the number of fishers of late 19^th century recreational charters, Thurstan et al. were able to expand the data set to 278 entries. This is was a success considering that between all media only 47 records were replete with all 3 of the variables necessary for calculating fishing effort.

Snapper are considered data deficient according to the IUCN Red List. In Queensland, Australia they are considered overfished. The designation from the local governing body there has caused great public debate. As Australia’s governing bodies mull over how best to proceed, similar stories are unraveling worldwide. If the information we have available to us on fishery abundance is at best piecemeal, Thurstan et al.’s research breathes new hope into looking back so that we may go forward.

Nineteenth century narratives reveal historic catch rates for Australian snapper (Pagrus auratus) Ruth H Thurstan, Alexander B Campbell, & John M Pandolfi DOI: 10.1111/faf.12103

Rising Ocean CO2 Levels are Hurting Cephalopods

March 11, 2015/0 Comments/in Conservation, Ocean News /by aanstett

by Jessica Wingar, RJD intern

In the last decade, the concerns of how global climate change is going to affect our planet have grown. One of the main components of what is causing this climate change is the increase in carbon dioxide in our environment. There was a major increase in carbon dioxide in the atmosphere after the industrial revolution. The level of carbon dioxide in the atmosphere has risen from 280ppm to 390ppm. The carbon dioxide from the atmosphere diffuses into the ocean, which has created an increase in carbon dioxide in the ocean. With the increasing carbon dioxide levels in the ocean, the pH of the ocean will decrease leading to many detrimental effects on the animals that live there. It is predicted that by 2300 the carbon dioxide levels in the ocean will be around 1900 μAtm, which will cause the pH of the ocean to drop by 0.77. This decrease in pH will cause extreme changes in the ocean and how organisms develop and survive under these conditions is of utmost importance (Heuer, R., 2014). One of the many classes that has been studied is cephalopoda. The cephalopods include such animals as squid, cuttlefish, and octopus. They are a very important class to ocean trophic levels and to the economy and it is essential to determine what negative effects will occur to them in the coming years (Kaplan, M.B., 2013).

One of these economically important species is Doryteuthis pealeii, the longfin squid. Squid are a critical part of the food chain in the ocean because not only do they serve as prey for many organisms, such as tuna, but they also serve as predators of many organisms. In a study conducted in 2013, this certain species of squid was used. D. pealeii lives in shallow waters in coastal regions. In this study, individuals were taken from Vineyard Sound, Massachusetts on two separate occasions during their breeding seasons which lasts from May to August. The aim of this study was to calculate the difference in mantle size, statolith size, statolith characteristics, and hatching time between control embryos and embryos at an elevated carbon dioxide level of about 2200 μAtm. This is slightly above the predicted levels for the year 2300. The study found that in both trials, embryos hatched later in the carbon dioxide treatment than the control embryos. For example, in the first trial on the first day of hatching, 62.6% of embryos hatched, whereas only 0.7% of the embryos with increased carbon dioxide hatched. The negative effects of this delay may be that there is an increased chance for predation.

Picture 1: Embryo hatching times for both trials

In addition to the hatching time, there were also many other negative changes in other parts of the squid. When the mantle length was looked at between the two conditions, the mantle was significantly shorter when the squid was reared in the carbon dioxide conditions. With a shorter mantle, the squid has less ability to move. Therefore, a shorter mantle can lead to slower swim speeds and lower migration causing a smaller chance of survival. Squid also have statoliths, which are calcified structures that are critical in balance and how the animal moves in the water. Seeing as these are calcified structures, their formation is greatly related to the acid content in the water. In this study, it was found that the statoliths of the squid in carbon dioxide had decreased surface area and a greater likelihood of abnormal shape and abnormal porosity. With decreased function of the statolith, the squid cannot orient itself the correct way in the water and again has decreased survival (Kaplan, M.B., 2013). Along with this type of cephalopod, cuttlefish also show a change in an inner calcareous structure in increased carbon dioxide conditions.

Picture 2: Average statolith surface area in the control treatment vs. the carbon dioxide treatment

Some cuttlefish have a calcareous structure called a cuttlebone that is located dorsally that goes from just behind the head to the end of its body. The purpose of this bone deals with buoyancy. During the day, the chambers of the cuttlebone are filled with fluid, which make the cuttlefish able to sink, and at night this fluid is expelled, which causes the cuttlefish to stay in the same place in the water column. A study done on Sepia officinalis, the common cuttlefish, looked at morphological changes in the cuttlebone in a carbon dioxide rich environment. In this study they found that carbon dioxide exposed cuttlebones had significantly less height and length, but had a 20-55% increase in mass. The shorter height can be accounted for by the fact that the lamellae in the cuttlebone in the carbon dioxide treatment were a lot closer together, compacting the cuttlebone. In addition, the inner pillars of the cuttlebone were found to have doubled in thickness, showing a build up of carbonate and an increase in mass. A heavier cuttlebone is detrimental to a cuttlefish because in order for that structure to control buoyancy it needs to be as light as possible; the cuttlefish will not be easily able to move up the water column because it will take more work to make the animal neutrally or positively buoyant. In addition, it will be more difficult for the cuttlefish to maintain a position in the water column while hunting, which could cause starvation in the organism (Gutowska, M.A., 2010).

Average cuttlebone measurements in the control vs. carbon dioxide treatments

Research into the consequences of ocean acidification is increasingly necessary in order to determine what will happen to the ocean in the next few hundred years. The spike in the carbon dioxide content in the oceans has been directly caused my humans and it is imperative that now something is done to slow down this increase.

References
Gutowska, M.A., Melzner, F, Pörtner, H.O., and Sebastian Meier. (2010). Cuttlebone calcification increases during exposure to elevated seawater pCO2 in the cephalopod Sepia officinalis. Marine Biology, 157 (7): 1653-1663.

Heuer, R.M., and Martin Grosell. (2014). Physiological impacts of elevated carbon dioxide and ocean acidification on fish. American Journal of Physiology, 307 (9): R1061-R1084.

Kaplan, M.B., Mooney, T.A., McCorkle, D.C., and Anne L. Cohen. (2013). Adverse Effects of Ocean Acidification on Early Development of Squid (Doryteuthis pealeii). PLOS ONE, 8 (5): 1-10.

Offshore Windmill’s Impact on the Marine Environment

March 4, 2015/0 Comments/in Conservation, Ocean News /by aanstett

by James Keegan, RJD intern

Global demand for renewable energy is increasing as nations strive to decrease their carbon emissions, pollution, and dependence on non-renewable resources like coal or oil. Because of its energy output and potential to compete in energy markets, wind energy may be the most promising renewable energy (IEA 2013). Consequently, wind energy has been rapidly expanding, reaching a capacity in 2012 that was 5 times greater than the capacity in 2005 (IEA 2013). Expectations for offshore wind energy are particularly high, as wind conditions are often stronger and more stable over sea (Bergström et al. 2014). Moreover, offshore wind farms allow for higher total levels of energy production and larger windmill units, which may be transported and constructed more easily (Bergström et al. 2014). Offshore wind farms also appease dissenters who contest that the visual disturbance caused by windmills ruins the aesthetics of local landscapes. As technology has advanced, the average capacity of turbines and size of offshore wind farms have been increasing, and they are being installed in deeper waters further from the coast (Bailey et al. 2014). By the end of 2013, operational wind farms were in an average water depth of 16 meters (~52 ft.) and 29 kilometers (~18 miles) from shore in Europe (Bailey et al. 2014). With such an increase in the encroachment on the marine environment, the focus on offshore wind farms’ impact on the local marine ecosystem continues to grow as well.

Windmill park in Oresund between Copenhagen, Denmark and Malmo, Sweden. (Photo source: Wikimedia Commons)

Although conservationists are studying the impact of offshore wind farms, the novelty of the technology and construction processes make it difficult to identify and quantify all of the stressors. The first commercial scale offshore wind farm, Horns Rev 1, only became operational in 2002 (Bailey et al. 2014). Moreover, the impact offshore wind farms have depends on local ecosystems, which can vary wildly. However, the understanding of the potential effects of offshore wind farms on marine ecosystems, as well as marine biodiversity, is steadily improving as empirical evidence from operational wind farms accumulates (Bergström et al. 2014). The two phases of offshore wind farms, construction and operation, have different potential effects, and these effects differ among species, depending on their likelihood of interaction with the structures and cables, sensitivities, and avoidance responses (Bailey et al. 2014). The major environmental concerns related to offshore wind farms are increased noise levels, risk of collisions, changes to benthic and pelagic habitats, alterations to food webs, pollution from increased vessel traffic, bird collisions, electromagnetic fields, and release of contaminants from seabed sediments (Bailey et al. 2014). However, offshore windmill farms also benefit the local ecosystem by acting as artificial reefs as well as de-facto marine reserves, providing protection against fishing pressures. With both beneficial and adverse contributions to the marine environment, offshore wind farms continue to intrigue conservationists.

Figure 2: An overview of the main pressures from offshore wind farms during the operational phase. Expected effect on the local abundance of marine organisms is indicated as (+) aggregation/increase, or (−) avoidance/decrease (Bergström et al. 2014).

The two fundamental stages of the development and use of offshore wind farms provide their own challenges and have their own environmental concerns. The construction phase is likely to have the greatest impact on marine mammals, and the activities of greatest concern are pile driving and increased vessel traffic (Bailey et al. 2014). Pile driving is the mechanical process of imbedding poles into sediment to provide foundational support for the proposed structure. Pile driving is currently the most common method used to secure turbine foundations to the seafloor, and it emits a considerable amount of noise (Bailey et al. 2014). The sounds emitted during pile driving could potentially cause hearing damage, mask calls, or displace animals as they leave the area to avoid the noise (Bailey et al. 2014). Moreover, the noise produced by pile driving can cause mortality and tissue damage in fish (Bergström et al. 2014). Alternatively, wind farms can use gravity foundations, which anchor windmills essentially by means of their own weight. The intensity of the noise caused by their installation is low, and animals are likely to return soon after the exposure has ended, thus lowering the impact (Bergström et al. 2014). However, this type of installation does cause high sediment dispersal due to dredging, or the removal of underwater sediments, but typically organisms inhabiting the sites of gravity foundation wind farms are tolerant of turbidity (Bergström et al. 2014). In addition to the installation of the windmills themselves, the increased vessel traffic associated with surveying and installation activities also creates the risk of collision and noise disturbance to marine mammals, sea turtles, and fish (Bailey et al. 2014). Although the construction phase of offshore wind farms only creates problems for the marine environment, its impact can be curtailed by avoiding significant habitats and seasons.

The operational phase of offshore wind farms requires a more challenging and complex assessment because of the duality of its environmental impacts. Like the construction phase, the operational phase raises concerns about acoustic disturbances, but from electricity generation and boat traffic for service and maintenance. The acoustic disturbances caused by the operation of the windmills are within the hearing range of fish and mammals, but underwater sound levels are unlikely to reach dangerous levels or mask acoustic communication of marine mammals (Bergström et al. 2014), (Bailey et al. 2014). Transmission cables transporting the generated electricity produce electromagnetic fields, which can affect cartilaginous fish, like sharks, which use electromagnetic signals in detecting prey (Bergström et al. 2014). The electromagnetic fields could also disturb fish migration patterns by interfering with their capacity to orientate themselves in relation to Earth’s magnetic field (Bergström et al. 2014). However, the production of these electromagnetic fields can be mitigated by proper cable design (Bergström et al. 2014). The major concerns for this phase of offshore wind farms are seabird mortality caused by collision with the moving turbine blades and seabird displacement from key habitats as a result of avoidance responses (Bailey et al. 2014). These issues can affect birds migrating through the area as well as those that breed or forage in the vicinity.

Although the operation of offshore windmills has negative impacts on the local ecosystem, these impacts may be matched or even outweighed by the positive ones that wind farms also introduce. Windmills can produce habitat gain by acting as artificial reefs, thereby enhancing local species abundances and biodiversity (Bergström et al. 2014). Moreover, studies have found that fish are seasonally attracted to wind farms with high fidelity, and that seals are potentially using wind farms as foraging sites (Reubens et al. 2014), (Russell et al. 2014). However, increased species abundance can be problematic when some species benefit more than others, or when wind farms introduce non-indigenous species (Bergström et al. 2014). Another major positive contribution wind farms make to the local ecosystem is fisheries exclusion. Although wind farms restrict fisheries’ intrusions for the safety and preservation of the farm itself, the local species benefit, both targeted species and non-targeted bycatch species (Bergström et al. 2014). This exclusion also prevents bottom trawling, the dragging of nets on the sea floor, so benthic organisms benefit as well (Bergström et al. 2014). Moreover, an abundance of fish caused by the exclusion of fisheries may have spillover, and surrounding areas may also see an increase in species abundance (Bergström et al. 2014). There may also be opportunities in the future to combine offshore wind farms with open ocean aquaculture (Bailey et al. 2014). With notable contributions to biodiversity and species abundance, windmill farms mitigate their negative impacts on the local environment.

With an increasing demand for renewable energy and, by extension, wind energy, offshore wind farms will continue to develop and grow around the world. Therefore, an increasing understanding of the impacts offshore wind farms have on marine environments is needed. Currently, investigations show that the construction phase consistently inflicts negative impacts, and that pressures during the operational phase may impose both negative and positive effects, depending on local environmental conditions as well as prevailing management targets (Bergström et al. 2014). However, confidence in these findings is not perfect because of their variable nature and because of the relatively short time frame offshore wind farms have operated, limiting data collection. In order to gain a better understanding of potential impacts, conservationists need to further investigate population dynamics and migrations in areas that already have wind farms and areas that are under consideration for them.
References:

IEA (2013), World Energy Outlook 2013, IEA. doi: 10.1787/weo-2013-en
Bergström, L., Kautsky, L., Malm, T., Rosenburg, R., Walberg, M., Capetilli, N. Å., and Wilelmsson, D. (2014) Effects of Offshore Wind Farms on Marine Wildlife – A Generalized Impact Assessment. Environmental Research Letters, 9. doi:10.1088/1748-9326/9/3/034012

Bailey, H., Brookes, K.L., and Thompson, P.M. (2014) Assessing Environmental Impacts of Offshore Wind Farms: Lessons Learned and recommendations for the Future. Aquatic Biosystems, 10:8. doi:10.1186/2046-9063-10-8

Reubens, J.T., Degraer, S., and Vincx, M. (2014) The Ecology of Benthopelagic Fishes at Offshore Wind Farms: A Synthesis of 4 Years of Research. Hydrobiologia, 727: 121-136. doi:10.1007/s10750-013-1793-1

Russell, D.J.F., Brasseur, S.M.J.M., Thompson, D., Hastie, G.D., Janik, V.M., Aarts, G., McClintock, B.T., Matthiopoulous, J., Moss, S.E.W., and McConnell, B. (2014) Marine Mammals Trace Anthropogenic Structures at Sea. Current Biology, 24(14): R638- R639. doi:10.1016/j.cub.2014.06.033

The Understanding of Giant Clams’ Contributions to Coral Reef Health Continues to Grow

February 27, 2015/0 Comments/in Conservation, Ocean News /by aanstett

by James Keegan, RJD intern

Coral reefs suffer from a multitude of problems, such as global warming and ocean acidification, which can be deadly for the reefs. Other issues, like losing individual species, although troublesome, do not garner the same attention because they do not cause as much harm. However, each reef organism has their role to play in the ecosystem, and because of their wide range of functions and highly threatened status, giant clams may deserve special consideration. Currently, the 13 known species of giant clams live in the Indo-West Pacific. The largest species, Tridacna gigas, can reach shell lengths of 120 cm (~3 ft 11 in) and weights in excess of 200 kg (~441 lbs). Because of their high tissue mass and heavy calcified shells, humans have been using them for both food and building material. Along with this demand, habitat degradation, technological advances in exploitation, and expanding trade networks have decreased giant clam numbers throughout their range. Moreover, giant clams are especially vulnerable to this sort of depletion because of their late sexual maturity, sedentary lifestyle, and external fertilization through broadcast release of reproductive cells. Fertilization success requires a sufficient number of spawning individuals, and low densities result in reduced, or zero, juvenile survival and eventual population collapse.

Although giant clams are protected under international law, their stocks are declining rapidly in many countries, and local extinctions are occurring. Such losses could have an unknown number of consequences because giant clams’ significance in coral reefs is not well understood. Giant clams serve several ecological functions in coral reef ecosystems, but conservationists have not previously assessed the extent to which these functions impact the local ecosystem. To rectify this, Neo et al. 2015 used data from literature and their own studies to determine a more accurate assessment of the role giant clams play in coral reefs.

Neo et al. 2015 sought out to properly establish and quantify giant clams’ contribution to reef ecosystems. They used the data obtained from the literature to consolidate information as well as calculate parameters like population density, size distribution, biomass, shell weight, and production. They found that giant clams provide food for local organisms directly through their tissue and indirectly through the discharge of feces, gametes (reproductive cells), and zooxanthellae (photosynthetic algae). Other organisms can also take up and host the zooxanthellae that giant clams expel.

Figure 1: Maximum net primary productivity (NPP) of different reef flora and fauna, measured in terms of net oxygen production (units are in terms of grams of oxygen produced per meter squared per day). The two giant clam species listed have the second and third greatest NPP, beating out hard corals and most algae. (Neo et al. 2015)

Furthermore, the shells of giant clams provide a surface for colonization by epibionts, organisms that live on the surface of other living organisms. An example of an epibiont would be a barnacle. Giant clams serve as nurseries and refugees for fish on the reef as well, and they can even shelter anemone fish in the absence of host anemones. The space between the outer wall of the clam’s soft body and its internal organs, known as the mantle cavity, also provides a habitat for symbiotic organisms.

Figure 2: Epibiota diversity among giant clam species. The ones shown on the giant clams in each picture are: (a) another clam (b) hard coral (c) algae and (d) a variety of encrusting organisms. (Neo et al. 2015)

Moreover, giant clams counteract eutrophication, the nutrient enrichment of water that typically leads to excessive algal growth, by filtering the water and sequestering nutrients. Giant clams also contribute to the topographic relief of reefs, which in itself modifies or creates habitat and affects local water flow. This alteration in water flow benefits the reef by hindering sedimentation and improving food influx. Finally, giant clams make their shells out of calcium carbonate, the same material hard corals use for their skeletons, so their shell material can be incorporated into the reef framework.

Giant clams benefit coral reefs in many ways, and their presence is indicative of reef health. Unfortunately, overfishing has put giant clams under great pressure, and their local extinction could be detrimental to coral reefs. By enhancing the understanding of giant clam contributions to coral reefs, Neo et al. 2015 hope to reinforce the case for their conservation.

References

Neo, M.L., Eckman, W., Vicentuan, K., Teo, S.L.-M., Todd, P.A. (2015) The Ecological Significance of Giant Clams in Coral Reef Ecosystems. Biological Conservation, 181: 111-123. doi:10.1016/j.biocon.2014.11.004