The Invasion of Centrostephanus Rodgersii in Tasmania

MSCI5005: Topics in Marine Science

Kerwin C. Ferrer Z3444817 20/05/2013 Submitted to: Prof. Iain Suthers

Abstract
The strengthening of the East Australian Current has resulted in a range extension of species towards Tasmania. An example of this is the diadematide sea urchin, Centrostephanus rodgersii which was historically found in New South Wales only. Aside from the strengthening of the EAC, the sea urchin was able to successfully migrate into its new habitat in Tasmania because of overfishing of large predators and thereby decreasing the resilience of macroalgal habitats. The effects of the invasion of the C. rodgersii is alarming because of its overgrazing which transforms healthy macroalgal habitats into sea urchin barrens resulting to a loss of biodiversity. The transformation of macroalgal habitats into barrens also has a negative effect in the abalone and rock lobster industry which contribute to around $160 or 94% of the wild catch sector of the Tasmanian fisheries. Looking into population dynamics such as age, growth and reproduction, it was found out that the recruitment of C. rodgersii from its historical range is still continuous and that its reproductive capability in Tasmania is higher compared to that of its counterpart in New South Wales. It is predicted that the strengthening of the EAC will continue in the future and that an increase in temperature in the Tasman area is also expected. The strengthening of the EAC will facilitate in the further transport of larvae from its historical range while the increase in temperature in the Tasman area will aid in the larval development of the C. rodgersii which has a temperature threshold of 12C. Future increase in population of C. rodgersii is therefore expected and this may lead to wide spread barrens that may cover 50% of the near shore rocky reef areas as also seen in New South Wales. Management options include the culling of sea urchins by abalone divers and the introduction and preservation of large predators such as the rock lobster Jasus edwardsii into Marine Protected Areas. The

data from the release of large lobsters can then be used to create an ecosystem model that will identify the minimum population of rock lobsters needed to prevent the sea urchin from forming barrens. Another possible option is the expansion of the market for sea urchin roe which will not only help in decreasing the number of sea urchins but also provide a sustainable source of food.

Contents Introduction ...................................................................................................................................... 1 The Centrostephanus Rodgersii ....................................................................................................... 1 Discovery of range extension........................................................................................................... 2 Causes of range extension ................................................................................................................ 3 Strengthening and penetration of the East Australian Current into Tasmanian waters ............... 3 Overfishing ................................................................................................................................... 4 Effects of the range extension of C. rodgersii ................................................................................. 5 Overgrazing results to barrens...................................................................................................... 5 Decrease in taxa diversity ............................................................................................................ 6 Effect in the abalone and lobster fishery ...................................................................................... 6 Population dynamics and future implications .................................................................................. 7 Preventive measures and Management options ............................................................................. 10 Conclusion ..................................................................................................................................... 12 References ...................................................................................................................................... 13

Introduction
Climate change has started to affect the southeastern coast of Australia. This is seen in the 350 km southwards extension of the EAC towards Tasmania (Ridgway 2007). Several marine species were observed to have started a poleward range extension into Tasmanian waters and the sea urchin Centrostephanus rodgersii is one of the controversial species because of its catastrophic behavior of altering healthy and diverse habitats into sea urchin barrens (Ling 2008). In this essay, firstly, we will look into the factors that paved way to the successful invasion of the sea urchin into Tasmania. Secondly, find out the effects of its migration to the existing marine ecosystem. Thirdly, predict what we may expect in the future and finally, tackle on the management options that can be used to prevent a catastrophic invasion of the sea urchin.

The Centrostephanus Rodgersii

The Centrostephanus Rodgersii is a species of sea urchin that belongs to the family diamatidae. Historically, this species of sea urchin was only native to New South Wales, but in the past decades, it has started to propagate and increase its population towards Tasmania, where it was never before seen (Johnson et al. 2005).. C. rodgersii is commonly found in the rocky subtidal reefs of New South Wales. It is often found in large assemblies that can reach up to 60 urchins per square meter (Andrew & Byrne 2007). Its diet consists of seaweeds, algae, byrozoans and sponges and is mostly active and grazes during night time (Miskelly 2002, p.30). In its historical range (New South Wales), the spawning period of the C. rodgersii starts in Winter, at around June and may last several months depending on location such that spawning of populations in its northern limits would last a short 1 month period while those in the southern limit had longer spawning periods (Andrew & Byrne 2007). It was noted by Andrew & Byrne (2007) that gonad sizes of sea urchins found in the fringe habitat are usually
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higher than those that are living in the urchin barrens which may be caused by the amount of food available in each habitat. In a study conducted by Huggett et al. (2005) results showed that after successful fertilization and formation of an embryo, it would take around 55 hours before it comes to its early pluteus larval stage. During this time, it can be seen as a twoarmed larva because of its prominent long postoral arms while its anterolateral arms are relatively shorter. After 3 to 4 months, the larva then starts its metamorphosis into a juvenile urchin, where it becomes radially symmetrical and spines start to form.

Discovery of range extension

The presence of C. rodgersii off Tasmania was first discovered in 1978 in St Helens and it started to increase and move towards the south along the east coast of Tasmania (Johnson et al. 2005). Johnson et al. (2005) estimates that the poleward range extension of the sea urchin C. rodgersii may have started migration to Kent Island (island north of mainland Tasmania) in 1960 and as years and decades passed, it can now be found even in the southern parts of mainland Tasmania (see Figure 1). It now has a dense population in Eastern Tasmania where sea urchin barrens created by its overgrazing are also found in large numbers. The sea urchin barrens are very numerous in the Eastern side of Tasmania, but it decreases in number as the latitude increases. In the southern limit of the range extension of the C. rodgersii, only incipient barrens were observed (Johnson et al. 2005) which is probably because C. rodgersii has just started to populate the area.

Figure 1: The History of the migration of the C. rodgersii in Tasmania. From: Ling (2008)

Causes of range extension

Strengthening and penetration of the East Australian Current into Tasmanian waters

Several factors or stressors may have caused the successful invasion of this species into the Tasman area. First of this is the strengthening of the East Australian Current, which was observed from an increase in the Sea Surface Temperature in the Tasman area as observed by Ridgway (2007). Figure 2 shows the penetration of the EAC into the east coast Tasmania as evidenced by an increased temperature in that area. Because of the extension of the EAC into the Tasman area, C. rodgersii in its pelagic larval state was able to migrate into its new habitat (Johnson et al. 2005). C. rodgersii was found to have a larval stage of 3 to 4 months, where it is just floating in the water column for the said duration, enabling it to be transported to long distances (Huggett et al. 2005). The extension of the EAC also produced an increase in temperature in the said area which also supported the larval development of the C. rodgersii, which has a temperature threshold of 12 C (Johnson et al. 2005, Ling et al. 2008). This is an example of a climate change-induced range extension of a species.

Figure 2: The strengthening of the EAC and its penetration into Eastern Tasmania. From Ridgway (2007).

Overfishing

Another factor that contributed to the success of the migration of C. rodgersii in the Tasman area is the decrease of resilience of the rocky reef habitats due to overfishing (Ling et al. 2009a). Ling et al. (2009a) found out that the rock lobster (Jasus edwardsii), which can be found in the Tasman area is one of the main species that is able to prey on the C. rodgersii. In their study, adult sized J. edwardsii with a carapace length of more than 140 mm was able to prey on C. rodgersii with a test diameter of 60 mm. This predation was observed in the Marine Protected Areas, where the lobsters were not taken and disturbed. However, habitats outside of the MPAs, are experiencing an increase in C. rodgersii population due to the absence or minimal presence of J. edwardsii because it is being overfished in the said area. Because of the overfishing of the lobsters in Tasmania, foreign invasion of the C. rodgersii was not met with resistance.

Effects of the range extension of C. rodgersii

Overgrazing results to barrens

One of the main issues that is of most concern regarding the invasion of C. rodgersii in Tasman area is its formation of barrens. Johnson et al. (2011) emphasizes on this saying The critical issue associated with the advent of C. rodgersii in Tasmania is the formation of barrens habitat caused by their overgrazing of macroalgae and intense predation on a wide range of sessile benthic invertebrates (p. 27). In New South Wales, it was observed by Andrew & ONeill (2000) that barrens cover around 50 per cent of the near-shore rocky reef area which is dominantly due to the overgrazing of the C. rodgersii. Johnson et al. (2011) predicts the possibility that the same can happen in the rocky reef areas of the east coast of Tasmania. Widespread barrens were found at the northeastern parts of Tasmania where the C. rodgersii have been grazing for years and they were positively correlated to the presence of C. rodgersii (Johnson et al. 2005). In the southern limit where C. rodgersii was relatively new, a few incipient barrens are starting to occur (Johnson et al. 2005). Trasformation into barrens does not necessarily occur right after the arrival of the C. rodgersii but would usually take a decade or two. Ling and Johnson (2009) suggests that barrens formation is associated with relatively mature sea urchin populations, as widespread barrens are only currently observed at sites where the average population age is >18 yr (p. 122). They further add that an eventual growth in population of the sea urchin in the said area would also lead to the transformation from a macroalgal habitat to a sea urchin barren. Another interesting note is that to transform a macroalgal habitat into a sea urchin barren would require a higher population of C. rodgersii, however, to maintain a sea urchin barren would require less sea urchin density (Hill et al. 2003). This means that to be able to rehabilitate a sea urchin barren back to a macroalgal habitat would require a regular and massive harvesting or culling of sea urchins which Johnson et al. (2005) points out as not an easy task.

Decrease in taxa diversity

Another effect of the invasion of the C. rodgersii is the loss of biodiversity. A study by Ling (2008) looked into the effect of removing the C. rodgersii from incipient barrens in Tasmania. He found out that in incipient barrens where C. rodgersii was extracted, canopyforming microalgae such as Ecklonia radiata and Phylospora comosa started to occur in greater numbers than in incipient barrens where the C. rodgersii were undisturbed. Ling (2008) also states that The removal of C. rodgersii clearly increased taxonomic richness, total abundance and Shannon diversity of benthic fauna (p. 888). It was found out that barrens produced by C. rodgersii grazing resulted to a loss of around 150 taxa. Recovery of the macroalgal habitat from an incipient barrens state after removal of C. rodgersii resulted 15 months after the start of the study which is in contrast to what was observed in New South Wales experiments that resulted to slow recovery. The author further notes that patching up incipient barrens in Tasmania resulted to increased diversity because of the addition of grazer resistant taxa which was rarely observed in healthy macroalgal beds. The author concludes that range extension of habitat-modifying organisms would highly affect marine diversity.
Effect in the abalone and lobster fishery

The Tasmanian fisheries contribute the largest share in the fisheries production of Australia at 27 per cent amounting to $596.7 million in 2010-11 (ABARE 2012). This comprises of the aquaculture sector and wild-catch sector. The Abalone Fishery accounts for 58 per cent ($97 million) of the wild-catch sector while the rock lobster accounts for 36 per cent ($59.5 million). The abalone and rock lobster fisheries therefore are very important to the Tasmanian Fisheries production. However, due to the invasion of the C. rodgersii, the abalone (Haliotis rubra) and rock lobster (Jasus edwardsii), which are mainly found in macroalgal habitats, are in danger of being affected by the overgrazing activities of the newcomer sea urchin. In New South Wales, a negative relationship was observed between the

population of sea urchin to that of the abalone (Andrew et al. 1998, p.61). Similarly, this relationship was also seen in East Tasmania, where an increase in density of C. rodgersii led to a decrease in abundance not only of abalone, but also of lobsters (Johnson et al. 2011). This maybe because lobsters and abalone are not commonly found in barrens created by C. rodgersii, but in addition to that, Strain & Johnson (2009) found out that the abalone population in intact algal beds was also negatively affected by the presence of C. rodgersii even when barrens have not yet occurred. Widespread barrens have started to increase in number in the East coast of Tasmania which could lead to negative consequences on the lobster, abalone and other species that rely on the macroalgal habitat (Johnson et al. 2005).

Population dynamics and future implications

Predicting future developments of the range extension of C. rodgersii in Tasmania would be helpful in managing the and preparing solutions for the said problem. By looking into the population dynamics of the invading urchin we can infer possible future scenarios (Ling et al. 2009b) and therefore help in planning future management actions. Ling and Johnson (2009) studied the age and growth of the C. rodgersii from the macroalagal boundary habitat and recently formed barrens in northeastern Tasmania. They tagged around 300 C. rodgersii at each site by injecting tetracycline-HCL in the peristomial membrane (the oral area) of the urchin. The tetracycline creates stains in the jaw of the sea urchin, and after a year, the growth of the jaw can be measured by distinguishing the stained and the non-stained area of the jaw under UV light. An indeterminate growth pattern was observed on the change in jaw length and the initial jaw length of the sea urchin. This implies that as the jaw length grows longer, its growth rate becomes slower. A growth model is then created for each habitat (barrens and macroalgal boundary) and from this, the age of the sea urchins were then determined. In their study, sea urchins in the macroalgal habitat demonstrated a faster growth rate (in terms of test diameter, thickness and weight) than their contemporaries in the barrens

habitat. However, Ling & Johnson (2009) observed that the reproductive power of the sea urchin living in barrens did not decrease significantly as opposed to studies of C. rodgersii in New South Wales by Byrne et al. (1998). The same method was used by Ling et al. (2009b) where they developed a growth model for the C. rodgersii in eastern Tasmania. In their study, a wide variety of ages which include plenty of old aged C. rodgersii were observed in the northern parts of eastern Tasmania while younger populations were seen towards the south. Ling et al (2009b) states the broad range of C. rodgersii ages in NE Tasmania indicates that the range extension has not occurred as the result of a single, massive recruitment event (p. 725). This, they say shows that multiple recruitment events (with larvae coming from the historical range) contributed to the establishment of C. rodgersii in Tasmania and these migration events may be continually ongoing. Banks et al. (2010) also confirms this with the result of their genetic analysis on the C. rodgersii showing minimal genetic differences of the urchin population in Tasmania from that of mainland Australia (NSW) which dismisses the probability of a founder effect or a single massive migration. Ling et al. (2008) studied the reproductive cycle of C. rodgersii in Tasmania. Collecting samples every two months for a period of 18 months, they were able to identify the month of July and August as the spawning season of the C. rodgersii. This was inferred from a decrease in Gonad Index (GI) and an increase in the number of successful induced spawning in those months. The study also showed that the GI of C. rodgersii in Tasmania was higher compared to those in New South Wales which indicate a higher reproductive potential for the Tasmanian inhabitants. They inferred that this maybe due to the higher availability of food in macroalgal beds and the lower population density resulting to less food competition between urchins. Moreover, Ling et al. (2008) also observed that the temperature threshold for the development of the C. rodgersii embryo to its two-arm larval stage was

12C which also corresponds to the result of the study of King (1992), as cited by Ling et al. (2008), for the C. rodgersii found in New South Wales. This implies that the development of the C. rodgersii requires temperatures above 12C during winter time (time of spawning) which in recent years has shown exceedance of that value. The development of the C. rodgersii to a larva was also found to be faster with an increase in temperature. The continuous larval recruitment of the C. rodgersii from mainland Australia is evident from the studies of Ling et al. (2009b) and Banks et al. (2010). The reproductive potential of Tasmanian C. rodgersii seems to be high according to Ling & Johnson (2009) and Ling et al. (2008). It is also found that the C. rodgersii is able to complete its reproductive cycle when the temperature is above 12C during the time of spawning (Ling et al. 2008). Years of temperature data during winter time (Figure 3) shows an increasing trend which is primarily due to the penetration of the EAC into Tasmanian waters (Ridgway 2007). If this trend continues, an increase in temperature in Tasmanian waters will result in higher and faster reproduction capability of the C. rodgersii and a continuous supply of larvae from mainland Australia is expected.

Figure 3: Winter temperatures in eastern Tasmania since 1946 -2007. From Ling et al. (2008)

Preventive measures and Management options

The catastrophic shift from healthy macroalgal kelp beds into sea urchin barrens is one of the priorities that management must focus on. It seems that the range extension of the C. rodgersii towards the south will still continue especially that climate change is imminent. Therefore, to be able to prevent further damage to the marine ecosystem of Tasmania, several mitigation measures should be done. The Institute of Marine and Aquatic Studies (IMAS) has partnered with the Fisheries Research and Development Corporation (FRDC) and the Natural Resource Management (NRM) Program in a project called Centrostephanus project (Institute of Marine and Aquatic Studies 2011). Its aim is to evaluate possible options to prevent further barrens formation due to C. rodgersii overgrazing. One of the plans being implemented by the Centrostephanus project is the Culling of the C. rodgersii by divers which they call as Protect your patch. By this, professional divers while harvesting abalone as a livelihood are tasked to cull C. rodgersii urchins. They are assigned to specific areas where incipient barrens occur and have to take records every time they finish culling sea urchins and harvesting abalone. This area is then compared to another area where no culling took place and then find out if kelp bed recovery is observed. Another plan of the Centrostephanus project is the release of large lobsters in marine protected areas and evaluating the effect of the addition of lobsters through ecosystem modeling (IMAS 2011). Ling et al. (2009a) reported that the rock lobster J. edwardsii with >140mm carapace length is effective in preying on sea urchins. Furthermore, Ling and Johnson (2012) have pointed out the effectiveness of Marine Protected Areas in increasing resilience and decreasing the survival rate of C. rodgersii because of the presence of large predators such as J. edwardsii. If large number of lobsters is released in an area, it may facilitate in the control of the population of the C. rodgersii and may reduce the future

occurrence of sea urchin barrens. In 2008, before the creation of the Centrostephanus project and IMAS, the Tasmanian Aquaculture and Fisheries Institute already piloted the release of large lobsters in sea urchin barrens and found out that these lobsters were effectively eating the sea urchins (Ling et al. 2009c). Ling and Johnson (2012) further adds that an increase in size and population of rock lobsters and other predators of the C. rodgersii can also be attained by rotational spatial closures, managed predator relocation, upper size limits and/or catch reductions, allowing accumulation of large predator biomass on rocky reefs (p. 1242). Data from the release of large lobsters is then used to construct an ecosystem model to identify the minimum population of lobsters needed to control sea urchin populations and prevent barrens formation (IMAS 2011). Another option is the creation or expansion of the market for C. rodgersii roe. In New South Wales, Andrew et al. (1998) suggested the creation of a market for sea urchin roe (gonads) to be able to help decrease the C. rodgersii population and increase the abundance of abalone in the area. Not only does this help in minimizing the effects of the C. rodgersii to the marine ecosystem, it also creates a sustainable source of food. However, to be able to produce profitable and marketable sea urchins, the quality of roe should also be considered. Ling et al. (2008) and Andrew et al. (2007) pointed out that gonad sizes of C. rodgersii living in macroalgal beds or incipient barrens are relatively larger (better quality roe) than those living in urchin barrens. A seafood company in Tasmania has recently started harvesting and processing sea urchins roe quality is good (Norwood 2012). They are already supplying to the local Australian market and are planning to export their sea urchin roe to Japan, where demand for this product is large. The company will also start to supply a rock lobster fishermens association to look into the possibility of including the sea urchin roe into baits used to catch rock lobsters.

Certainly, the issue of the invasion of the C. rodgersii should be listed in the priority list for marine ecosystem managers in Tasmania. Ling et al. (2009a) further emphasizes on the importance of addressing this issue: Management must therefore aim to prevent further phase shifts to sea urchin barrens because the strong hysteresis effect makes rehabilitation of existing barrens to kelp beds exceedingly difficult (p. 22344).

Conclusion
It is evident that the C. rodgersii was able to successfully invade the East coast of Tasmania as seen in its continuous and unopposed migration. With a projected climate change, through the strengthening and extension of the EAC in East Tasmania(Ridgway 2007), the sea urchin will be able to continuously migrate from its historical range and into Tasmania. If the increase in temperature in Tasmania continues, the sea urchin will also be able to successfully reproduce and complete its life cycle and probably will be able to propagate southwards. The barrens formation of the sea urchin affects the marine ecosystem supported by the macroalgal beds, especially the valued abalone and the rock lobster fisheries (Johnson et al. 2005). If the invasion of the sea urchin continues resulting to widespread barrens in Eastern Tasmania, the fishing industry would suffer. Therefore, to be able to prevent this from happening, management action should be done such as culling of sea urchins, increasing the size and population of rock lobsters that are able to prey on the sea urchin and develop a market for sea urchin roe.

References
ABARE 2012. Australian Fisheries Statistics 2011, Australian Bureau of Agricultural and Resource Economics, Canberra, Australia. Andrew, NL & Byrne, M 2007. Ecology of Centrostephanus. In: Lawrence, J. M. (ed.) Edible Sea Urchins: Biology and Ecology. New York: Elsevier Science. Andrew, NL & O'Neill, AL 2000. 'Large-scale patterns in habitat structure on subtidal rocky reefs in New South Wales'. Marine and Freshwater Research, vol. 51, pp 255-263. Andrew, NL, Worthington, DG, Brett, PA, Bentley, N, Chick, RC & C, B 1998. Interactions between the abalone fishery and sea urchins in New South Wales, NSW Fisheries Research Institute. Banks, SC, Ling, SD, Johnson, CR, Piggott, MP, Williamson, JE & Beheregaray, LB 2010. 'Genetic structure of a recent climate changedriven range extension'. Molecular Ecology, vol. 19, pp 2011-2024. Hill, NA, Blount, C, Poore, AGB, Worthington, D & Steinberg, P 2003. 'Grazing effects of the sea urchin Centrostephanus rodgersii in two contrasting rocky reef habitats: effects of urchin density and its implications for the fishery'. Marine and Freshwater Research, vol. 54, pp 691-700. Huggett, MJ, King, CK, Williamson, JE & Steinberg, PD 2005. 'Larval development and metamorphosis of the australian diadematid sea urchin Centrostephanus rodgersii'. Invertebrate Reproduction and Development, vol. 47, pp 197-204. Institute of Marine and Aquatic Studies 2011. University of Tasmania, Australia, Accessed 28 April 2013, http://www.imas.utas.edu.au/research/marine-and-antarcticecosystems/urchin. Johnson, CR, Banks, SC, Barrett, NS, Cazassus, F, Dunstan, PK, Edgar, GJ, Frusher, SD, Gardner, C, Haddon, M & Helidoniotis, F 2011. 'Climate change cascades: shifts in oceanography, species' ranges and subtidal marine community dynamics in eastern Tasmania'. Journal of Experimental Marine Biology and Ecology, vol. 400, pp 17-32. Johnson, CR, Ling, S, Ross, D, Shepherd, S & Miller, K 2005. 'Establishment of the longspined sea urchin (Centrostephanus rodgersii) in Tasmania: first assessment of potential threats to fisheries'. FRDC Final Report, Project No. 2001/044. Fisheries Research and Development Corporation, Deakin West, ACT, Australia. King, CK. 1992. The reproduction and development of the Echinoid Centrostephanus rodgersii a potential bioassay organism. Honours Thesis, University of Sydney, Sydney. Ling, S 2008. 'Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state'. Oecologia, vol. 156, pp 883-894.

Ling, S & Johnson, CR 2009. 'Population dynamics of an ecologically important rangeextender: kelp beds versus sea urchin barrens'. Marine Ecology Progress Series, vol. 374, pp 113-125. Ling, S & Johnson, CR 2012. 'Marine reserves reduce risk of climate-driven phase shift by reinstating size-and habitat-specific trophic interactions'. Ecological Applications, vol. 22, pp 1232-1245. Ling, S, Johnson, CR, Frusher, S & King, CK 2008. 'Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range'. Global Change Biology, vol. 14, pp 907-915. Ling, S, Johnson, CR, Frusher, S & Ridgway, K 2009a. 'Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift'. Proceedings of the National Academy of Sciences, vol. 106, pp 22341-22345. Ling, S, Johnson, CR, Ridgway, K, Hobday, A & Haddon, M 2009b. 'Climatedriven range extension of a sea urchin: inferring future trends by analysis of recent population dynamics'. Global Change Biology, vol. 15, pp 719-731. Ling, S, Johnson, CR & Sanderson, J 2009c. 'Lobsters to fight urchin overgrazing?'. Fishing Today, vol. 22, pp 30-31. Miskelly, A 2002. Sea Urchins of Australia and the Indo-Pacific, Sydney, Australia, Capricornica Publications. Norwood, C 2012. 'Business Role for Wayward Urchins'. Fish, vol. 20, pp 16-19. Ridgway, K 2007. 'Longterm trend and decadal variability of the southward penetration of the East Australian Current'. Geophysical Research Letters, vol. 34. Strain, EM & Johnson, CR 2009. 'Competition between an invasive urchin and commercially fished abalone: effect on body condition, reproduction and survivorship'. Marine Ecology Progress Series, vol. 377, pp 169-182.