Heavy Metals Effect on the Fertilization and Development of Sea Urchin Embryos

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1 Heavy Metals Effect on the Fertilization and Development of Sea Urchin Embryos Kristin Parish, Jessica Brown, Renee Cook and Megan Kapp January 2012

2 Abstract Heavy metal pollution is a prevalent threat in aquatic systems, particularly in coastal regions where coast-side industries or large tributaries carrying pollutants introduce these toxins into the environment, necessitating bioindicators such as sea urchins to ascertain the toxicity of contaminants in the environment. In this experiment, sea urchins were used to test the effects of copper and zinc heavy metals on development. Concentrations of 8 ug/l, 24 ug/l, and 40 ug/l of copper and 40 ug/l, 400 ug/l, and 4,000 ug/l of zinc were used to examine the effects of these heavy metals on both fertilization and subsequent development over the next 72 hours. Data was recorded on the number of abnormalities and deaths compared to the total number of embryos for both copper and zinc. Copper was shown to cause a slight inhibition of fertilization at high concentrations and embryo development was impaired in its ability to form the vegetal plate as a blastula and its capacity for convergent extension in gastrulation. Zinc s affects were more dramatic, causing 100% death in the highest concentration of 4,000 ug/l and relatively low survivorship in the other two concentrations as well as abnormalities in blastopore formation and larval development. Copper was concluded to have a more toxic effect on development of embryos at a lower concentration, but less of an effect on the overall survivorship of the embryos. Introduction One of the greatest threats to the health of the environment today is the issue of pollution, particularly in aquatic ecosystems where pollutants can enter the system miles away and accumulate from multiple sources. Fertilizers, pesticides, industrial pollutants and waste byproducts are frequently discussed in terms of water pollution and their effects on the ecosystem. Of these pollutants, industrial wastes and their heavy metal byproducts are often overlooked from an environmental standpoint. When industries are located in areas near agricultural or recreational areas heavy metal pollution is considered a potential threat from the industry (Radeniac, Fichet, Miramand 2001). The threat of heavy metal poisoning on organisms in the ecosystem often seems to be overlooked; however, many of the negative effects of heavy metals on humans apply to organisms within the surrounding ecosystems. Heavy metals, such as copper, zinc, lead, mercury and nickel, can all act as poisons or teratogens, causing deformities or deaths in many organisms exposed to them. Organisms in aquatic systems, particularly smaller organisms, are often subject to heavy metal poisoning. When the metal is dissolved into the water column it becomes a significant aquatic contaminant that affects the organisms living within the ecosystem. Heavy metals can also settle in large quantities along river or coastal beds' sediment (Raeniac, Fichet, Miramand 2001). These heavy metals can be one of the most destructive anthropogenic pollutants. The effect of heavy metals on early development, particularly on early embryonic stages, can be detrimental to a species that occupies a habitat into which heavy metals are introduced. One organism that is easy to observe in development is the sea urchin, which lives in marine environments that are often subjected to heavy metal pollution, particularly in regions where there are coastal industries. Sea urchins are particularly susceptible to environmental conditions; in fact sea

3 urchins exposed to toxic conditions have inhibited embryonic development and growth (Quiniou, Guillou, Judas 1999). The fact that sea urchins respond so readily to environmental conditions makes them an ideal species to act as an indicator of ecosystem health. They are also one of the best bioindicators to determine heavy metal pollution because of the variety of developmental anomalies that are caused by the different heavy metals (Kabayashi and Okamaru, 2004). The objective of this experiment was to determine the toxicity of heavy metals in a variety of concentrations and what effect the metals had on the early development of sea urchin embryos. Two common heavy metal pollutants in aquatic ecosystems are copper and zinc metals. According to previous studies, low levels of zinc had no effect on the development of the sea urchin embryos, however concentrations of 140 ug/l caused abnormal development in embryos and the fertilization envelope was often deformed. In solutions of 480 ug/l of zinc, inhibitory effects on embryonic development were first observed (Kobayashi and Okamaru, 2004). Of these two heavy metals, copper is more harmful to embryo development (Kobayashi and Okamaru, 2005). Copper has been shown to cause multiple deformities at even at very low concentrations. Most of these abnormalities occurred in the gastrulation stage of development (Waterman, 1937). The experiment tested varying levels of both copper and zinc pollutants on sea urchin fertilization and embryo development; from low concentrations to approximately the concentrations where a developmental effect was observed in previously published studies. Observations of the sea urchin embryos were made at set intervals to observe all stages of development, beginning with fertilization. Abnormalities and fatalities of embryos were observed and recorded in order to determine the effects of the pollutants on the early development of the embryos and the concentration of the heavy metal pollutant needed to cause developmental defects. This experiment was performed for the purpose of determining the effect of the heavy metals copper and zinc on development of sea urchins in varying concentrations. Materials and Methods Preparation of Sea Urchin Embryos and Stock Solutions Three concentrations of each heavy metal were created and used to test the effects of the heavy metal on the development of sea urchin embryos. Copper concentrations of 8.0 ug/l, 24 ug/l and 40 ug/l were created to test the toxicity of copper as a heavy metal and observe the effects of the metal at different concentrations on both fertilization and development of the embryos. Copper concentrations were created by adding copper sulfate into artificial sea water. Zinc concentrations of 40 ug/l, 400 ug/l and 4,000 ug/l were used to test the effect of zinc on the embryos' fertilization and development. Zinc chloride added to and dissolved in artificial sea water for use in the experiment. All three concentrations of both zinc and copper were tested twice, along with two samples in artificial sea water to act as a control for variance that may occur in everyday fertilization and development. Zinc and copper concentrations were made through the use of serial dilutions to limit the amount of toxic waste resulting from the experiment.

4 Small Petri dishes were used to hold the concentrations and sea urchin embryos. For each sample, 10mL of that sample's artificial sea water solution was deposited into the dish to make a habitat for the subsequent sea urchin fertilization and embryos. Into this solution, 30uL of sea urchin eggs was deposited using a micropipette. Following this, 5uL of sea urchin sperm was deposited into the dish containing the artificial sea water solution and the sea urchin eggs. Observations Sperm were allowed to interact with eggs for 15 minutes, allowing fertilization to take place. 2uL were then extracted from the solution using a micropipette and places on a slide. The slide was viewed under a compound microscope at 10x power. Observations of the sperm and egg interactions were observed. In five random fields of view of each slide, the number of successful fertilizations was counted compared to the number of eggs present in the field of view. Any abnormalities that were observed were recorded. This procedure was repeated for each of the controls and heavy metal solution concentrations. The dishes were then wrapped in para-film to avoid loss of water from the system and the embryos were allowed to develop for 15 hours. After 15 hours, each of the embryos as observed in the same manner as fertilization was observed, 200uL of solution and embryos was drawn out of each dish and placed on a slide to be observed under the compound microscope. Again, five random fields of view were observed and observations were made. In the embryo stage, the number of embryos was counted and recorded. The number of embryo deaths or abnormalities was then observed and recorded. Abnormalities were described and a digital image was taken of the abnormality that occurred. Embryo observations also occurred at the 30 hour mark and the 72 hour mark in the same fashion. The time intervals were chosen to ensure that every stage of development was observed and development was recorded. The experiment was stopped at 72 hours because after 72 hours the embryo was well into the gastrula stage therefore the effects of heavy metals on early development had been well established.

5 Percent fertilization and abnormal development Results 1. Copper 100% Percent Successful Fertilization and Subsequent Percent Abnormal Development Observed 90% 80% 70% 60% 50% 40% 8 ug/l Copper 24 ug/l Copper 40 ug/l Copper 30% 20% 10% 0% Fertlization After 15 hours After 30 hours After 72 hours Fig. 1 Graph displaying the amount of successful fertilization taking place at varying concentrations of copper as well as the development of abnormalities over the course of the first 72 hours of development. The abnormalities observed after 15 hours encompassed the first stage of development (blastula stage) while the abnormalities observed after 30 hours include the second stage of development (gastrula stage) and the abnormalities observed after 72 hours occurred during the third stage of development (the larva stage). All observed control embryos successfully fertilized and none developed abnormalities. Increasing concentrations of copper appeared to slightly inhibit the success of fertilization, with no significant difference observed among the concentrations. However, copper did appear to significantly contribute to the abnormal development of sea urchin embryos compared to the control. None of the control eggs developed abnormalities, however, almost all stages of all concentrations showed some level of abnormalities (except 24 ug/l after 30 hours) as shown in Fig. 1. Abnormalities observed at the after 15 hour stage included a lack of blastopore for all abnormal embryos and overall the embryos appeared to be developing more slowly than the control at 8 ug/l. Embryos observed in the 24 ug/l solution presented with abnormal development in the vegetal plate after 15 hours with 2/3 of the abnormal embryos having no vegetal plate while the remaining 1/3 presented with a vegetal plate

6 that appeared much thinner than the control. At 40 ug/l, abnormalities observed included both abnormalities in the development of the blastopore (it developed outward rather than inward) and abnormalities in the vegetal plate formation similar to what was observed at 24 ug/l after 15 hours. Overall, the shape of the embryos in the blastula stage appeared rather flattened compared to the control at 40 ug/l after 15 hours. After 30 hours, embryos were still not fully developed with some still in the blastula stage and there was also a lack of skeletal rod development in some embryos at 8 ug/l. At 24 ug/l, no new abnormalities were observed after 30 hours, however developmental stages ranged from the beginning of germ layer formation to the pluteus larva stage to the larval stage similar to what was observed in the control. Abnormalities at 40 ug/l after 30 hours included thin vegetal plate, a disruption of the vegetal plate in the larva stage, and a shortening of the anterior head region of the larva. Embryos observed after 72 hours all appeared to have abnormalities in the convergent extension with the most extreme examples seen in increased concentrations of copper. Elongated tips were also observed at 8 ug/l while the anterior region of embryos in the 24 ug/l copper appeared pointed. Skeletal structures failed to properly develop in two of the embryos in the 40 ug/l concentration while the majority of the embryos displayed a short, stout appearance in the larval stage (Fig. 2). Fig. 2. Image shows a more normally developed pluteus (left) next to a pluteus (right) that developed with more abnormalities including a more stout appearance and possibly poor skeletal formation after 72 hours in a copper solution.

7 rcent successful fertilixation and abnormal development 2. Zinc 100% 90% 80% 70% Percent Successful Fertilization and Subsequent Percent Abnormal Development in the Presence of Zinc 60% 50% 40% 30% 40 ug/l Zinc 400 ug/l Zinc 4,000 ug/l Zinc 20% 10% 0% Fertilization After 15 hours After 30 hours After 72 hours Fig. 3 Graph illustrates the presence of abnormalities in sea urchin embryos in different concentrations of zinc over the first 72 hours of development following successful fertilization of an egg. Like copper, after 15 hours encompasses the first stage of development, after 30 hours encompasses the second stage of development, and after 72 hours encompasses the third stage of development. At 4,000 ug/l of zinc, no embryos made it past fertilization representing complete death.

8 Percent survivorship of embryos 100% Percent Survivorship of Embryos Following Successful Fertilization 90% 80% 70% 60% 50% 40% 0.04 g/l Zinc 0.4 g/l Zinc 4.0 g/l Zinc 30% 20% 10% 0% Fertilization After 15 hours After 30 hours After 72 hours Fig. 4. Graph demonstrates the percent survivorship of embryos at each of the developmental stages following successful fertilization at differing concentrations of zinc. Under differing concentrations of zinc both percent abnormality observed and survivorship were affected compared to the control (Fig.3 and Fig. 4). All concentrations of zinc appeared to reduce the success fertilization compared to the control, which had 100% success. In the first stage of development, only 40 ug/l produced any abnormalities with one embryo failing to develop a vegetal plate. At 40 ug/l and 400 ug/l, most of the embryos reached the blastula or gastrula stage after 15 hours. Survivorship was slightly impacted by the 40 ug/l and 400 ug/l of zinc in the first stage of development (Fig. 4) while no embryos were observed to have passed fertilization at the 4,000 ug/l concentration after 15 hours. After 30 hours, embryos in 40 ug/l zinc made it to the larva stage, but were observed having shorter stature than that of the control while 400 ug/l had a lack of blastopore formation compared to the control. Embryos observed after 72 in 40 ug/l appeared to be continuing to develop in the larva stage, but they appeared to have a shorter, rounder stature than those of the control while embryos in 400 ug/l appeared to have died or were all found the blastula stage developing extremely slowly (Fig. 5 and Fig. 6).

9 Fig 5. Image shows sea urchin embryo after 72 hours in 40 ug/l zinc solution. Larva stage is abnormal, resulting in shorter legs and a more rounded head appearance. Fig. 6. Image shows sea urchin embryo at late blastula/early gastrula after 72 hours in 400 ug/l zinc solution.

10 Discussion Heavy metal pollution in coastal aquatic zones is found across the globe, affecting nearby life forms in known and unknown ways. It is known heavy metals have deleterious effects on organism development, particularly in sea urchins. Within this experiment, even the lowest concentrations of copper and zinc which have been found within coastal aquatic regions in which sea urchins inhabit, were found to effect early embryonic development (Kobayashi and Okamura 2005). In the presence of both copper and zinc at varying concentrations, embryos failed to develop normally compared to controls with no added heavy metals. Additionally, zinc also had a significant impact on overall embryo survivorship with fewer embryos making it from one developmental stage to the next under all concentrations. Kobayashi and Okamura (2004 and 2005) found concentrations of zinc between ug/l had severe inhibitory effects on the development of a sea urchin embryo with embryos unable to surpass the blastula stage while concentrations between 14 and 58 ug/l resulted in a retarded gastrula stage and the presence of exo-gastrula. Results obtained in this experiment demonstrated similar abnormalities within the concentration ranges outlined by Kobayashi and Okamura (2005). Zinc likely restricts the development of the endoderm as well as mesenchyme derivatives, causing the abnormalities observed and leading to embryo death at higher concentrations (Timourian 1968). Copper appears to have a more toxic effect on sea urchin embryo development at lower concentration levels than zinc, however, overall survivorship is less impacted by copper than by zinc. Results obtained by Kobayashi and Okamura (2005) demonstrated that concentrations below 3.8 ug/l of copper produced normal development in the sea urchin embryo, but concentrations above 7.7 ug/l of copper produced significant abnormalities with little effect on survivorship. As Fig. 1 shows, most abnormalities were observed after 15 hours of development at all concentrations of copper, with most of the differences observed being in the development of the vegetal plate. Previous research indicates that copper disrupts gastrulation more than first cleavage or the blastula stage (Kobayashi 1980). However, the abnormalities observed in this study indicate that while embryos are able to complete the blastula stage, it is the abnormalities that begin in this stage with the thin vegetal plate that may contribute to the problems of convergent extension in gastrulation. Additionally, embryos in differing concentrations appeared to grow more slowly than the control embryos, indicating copper reduces the mitotic rate of the embryos (Palumbi 2004). Most notable, copper appears to greatly inhibit convergent extension of the sea urchin embryo with higher concentrations of copper having a more pronounced effect. Embryos in 40 ug/l of copper appeared much shorter and stouter than control counterparts, indicating a lack of archenteron elongation, possibly due to the failure of cells converging around the circumference of the archenteron leading to the lack of elongation to the animal pole. While individual effects of the heavy metal toxins impair embryos to differing degrees at each of the concentrations of copper and zinc, evidence is indicating that combining heavy metals can have synergistic effects on developing sea urchin embryos. Low levels of zinc appear to enhance the detrimental effects of other heavy metals such as copper and lead, however, it is still unknown how zinc amplifies the detrimental effects of other heavy metal toxins (Kobayashi and Okamura 2005). This has important implications for any effluent containing heavy metals that is entering water bodies, especially those that contain zinc. Even at low concentrations of contamination, development is still impacted

11 resulting in malformed organisms. Not only does this affect the overall success of organisms and populations such as sea urchins whose embryonic development is sensitive to low concentrations of contamination, it also potentially affects the food web that the sea urchins may play a critical role in and possibly represents a threat for human health as the heavy metals bioaccumulates through the food web. Thus, species such as sea urchins, which are readily impacted by slightly changes in metal contamination within the aquatic environment, may serve as ideal species for biomonitoring within the environment.

12 Works Cited Kobayashi, N Comparative sensitivity of various developmental stages of sea urchins to some chemicals. Marine Biology, 58: 3, Kobayashi, N., Okamura, H., Effects of heavy metals on sea urchin embryo development. 1. Tracing the cause by the effects. Chemosphere, 55, Kobayshi, N and Okamura H Effects of heavy metals on sea urchin embryo development. Part 2. Interactive toxic effects of heavy metals in synthetic mine effluents. Chemosphere, doi: /j.chemosphere Palumbi, L The effects of toxins on sea urchin embryo development. Stanford University, presentation. Radenac, Fichet and Miramand. "Bioaccumulation and toxicity of four dissolved metals in Paracentrotus lividus sea-urchin embryo." Marine Environmental Research 51 (2001): Print. Timourian, H The effect of zinc on sea urchin morphogenesis. Journal of Experimental Zoology, 169: doi: /jez Quiniou, Guillou, and Judas. "Arrest and Delay in Embryonic Development in Sea urchin Populations of the Bay of Brest (Brittany, France): Link with Environmental Factors" Marine Pollution Bulletin 38.5 (1999): Print. Waterman, A. J. "Effect of salts of heavy metals on development of the sea urchin, Arabacia punctulata" The Biological BulletinLXXIII.3 (1937): Print.

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