Tropical bivalves in extreme storms : Survivorship and filtration in response to salinity


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Tropical bivalves in extreme storms : Survivorship and filtration in response to salinity

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Tropical bivalves in extreme storms : Survivorship and filtration in response to salinity
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Bivalvos tropicales en tormentas extremas: sobrevivencia y filtración en respuesta a cambios de salinidad
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Hudson, Haley
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Bivalve water filtration provides important ecosystem services that can help to offset anthropogenic pollution and other human induced ecosystem imbalances. Pinctada mazatlanica, Pteria sterna, and Modiolus capax are bivalves that grow on fish mariculture nets filtering fish feces from the water. Bivalves can help make fish mariculture a more sustainable alternative to overfishing. However, freshwater from extreme storms threaten these species. Tropical Storm Nate caused salinity changes in marine ecosystems resulting in widespread destruction. Little was known about how Tropical Storm Nate affected bivalves. In my study, I addressed the question: How are survivorship and filtration rates of Pinctada mazatlanica, Pteria sterna, and Modiolus capax affected by salinity changes? I exposed nine replicates of Pinctada mazatlanica, Pteria sterna, and Modiolus capax to fresh, brackish, and saltwater, then tested for wáter filtration ability, and survivorship. Fresh and brackish water reduced survivorship after 24 hours for Pteria sterna, and after 48 hours for Pinctada mazatlanica and Modiolus capax. In addition, Pteria sterna survived for less time across all treatments. Modiolus capax had the highest survivorship in freshwater after 48 hours. These species can filter silt from saltwater, but not fresh or brackish water. Depending on the duration and severity of the tropical storm, most of my study species are likely to die from the freshwater. If they survive however, they can help the ecosystem recover after a storm by filtering excess silt out of saltwater. ( ,, )
Abstract:
La filtración de agua que realizan los bivalvos proporciona importantes servicios ecosistémicos que pueden ayudar a compensar la contaminación antropogénica y otros desequilibrios de los ecosistemas inducidos por el hombre. Pinctada mazatlanica, Pteria sterna y Modiolus capax son bivalvos que crecen en las redes de maricultura de peces y filtran las heces de los peces en el agua. Los bivalvos pueden ayudar a que la maricultura de peces sea una alternativa más sostenible que la sobrepesca. Sin embargo, el agua dulce de las tormentas extremas amenaza a estas especies. La tormenta tropical Nate provocó cambios en la salinidad de los ecosistemas marinos que causaron una destrucción generalizada. Se sabe poco acerca de cómo la tormenta tropical Nate afectó a los bivalvos. En mi estudio, abordé la pregunta: ¿Cómo afectan los cambios de salinidad a las tasas de sobrevivencia y filtración de Pinctada mazatlanica, Pteriasterna y Modiolus capax? Expuse individuos de Pinctada mazatlanica, Pteria sterna y Modiolus capax en nueve réplicas en tres tratamientos: agua dulce, salobre y salada. Luego, medí la capacidad de filtración de agua y la sobrevivencia. El agua dulce y salobre redujo la sobrevivencia de Pteria sterna después de 24 horas, y después de 48 horas se redujo la de Pinctada mazatlanica y Modiolus capax. Además, Pteria sternasobrevivió durante menos tiempo en todos los tratamientos. Modiolus capax tuvo la mayor sobrevivencia en agua dulce después de 48 horas. Estas especies pueden filtrar limo de agua salada, pero no agua dulce o salobre. Dependiendo de la duración y la severidad de la tormenta tropical, es probable que la mayoría de las especies estudiadas mueran a causa del agua dulce. Sin embargo, si sobreviven, pueden ayudar a que el ecosistema se recupere después de una tormenta filtrando el exceso de sedimento del agua salada.
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Student afiliation : Department of Evolution and Ecology; University of California, Davis
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Hudson !"! ! Tropical Bivalves in Extreme Storms: Survivorship and Filtration in Response to Salinity Changes Haley A. Hudson Department of Evolution and Ecology University of California, Davis EAP Tropical Biology and Conservation Program Spring 2019 7 June 2019 ABSTRACT Bivalve water filtration provide s important ecosystem services that can help to offset anthropogenic pollution and other human induced ecosystem imbalances. Pinctada mazatlanica , Pteria sterna, and Modiolus capax are bivalves that grow on fish maricu lture nets filtering fish feces from the water. Bivalves can help make fish mariculture a more sustainable alternative to overfishing . However, freshwater from extreme storms threaten these species . Tropical Storm Nate caused salinity changes in mari ne ecosystems resulting in widespread destruction. Little was known about how Tropical Storm Nate affected bivalves . In my study, I addressed the question: How are survivorship and filtration rates of Pinctada mazatlanica , Pteria sterna , and Modiolus capax affected by salinity changes? I exposed nine replicates of Pinctada mazatlanica , Pteria sterna , and Modiolus capax to fresh, brackish, and saltwater , then tested for water f iltration ability, and survivorship. Fres h and brackish water reduced survivorshi p after 24 hours for Pteria sterna , and after 48 hours for Pinctada mazatlanica and Modiolus capax . In addition, Pteria sterna survived for less time across all treatments. Modiolus capax had the highest survivorship in freshwater after 48 hours. These species can filter silt from saltwater, but not fresh or brackish water. Depending on th e duration and severity of the t ropical storm, most of my study species are likely to die from the freshwater. If they survive however, they can help the ecosystem reco ver after a storm by filter ing excess silt out of saltwater. Bivalvos tropicales en tormentas extremas: sobrevivencia y filtraci—n en respuesta a cambios de salinidad RESUMEN La filtraci—n de agua que realizan los bivalvos proporciona importantes servicios ecosistŽmicos que pueden ayudar a compensar la contaminaci—n antropogŽnica y otros desequilibrios de los ecosistemas inducidos por el hombre. Pinctada mazatlanica , Pteria sterna y Modiolus capax son bivalvos que crecen en las redes de maricultura de peces y filtran las heces de los peces en el agua. Los bivalvos pueden ayudar a que la maricultura de peces sea una alternativa m‡s sostenible que la sobrepesca. Sin embargo, el agua dulce de las tormentas extremas amenaza a estas especies. La tormenta tropical Nate provoc— cambios en la salinidad de los ecosistemas marinos que causaron una destrucci—n generalizada. Se sabe poco acerca de c—mo la tormenta tropical Nate afect— a los bivalvos. En mi estudio, abordŽ la pregunta: ÀC—mo afectan los cambios d e salinidad a las las tasas de sobrevivencia y filtraci—n de Pinctada mazatlanica , Pteria sterna y Modiolus capax ? Expuse individuos de Pinctada mazatlanica , Pteria sterna y

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Tropical Bivalves in Extreme Storms Hudson # ! Modiolus capax en nueve rŽplicas en tres tratamientos: agua dulce, salobre y salada. Luego, med’ la capacidad de filtraci—n de agua y la sobrevivencia. El agua dulce y salobre redujo la sobrevivencia de Pteria sterna despuŽs de 24 horas, y despuŽs de 48 horas se redujo la de Pinctada mazatlanica y Modiolus capax . Adem‡s, Pteria ste rna sobrevivi— durante menos tiempo en todos los tratamientos. Modiolus capax tuvo la mayor sobrevivencia en agua dulce despuŽs de 48 horas. Estas especies pueden filtrar limo de agua salada, pero no agua dulce o salobre. Dependiendo de la duraci—n y la sev eridad de la tormenta tropical, es probable que la mayor’a de las especies estudiadas mueran a causa del agua dulce. Sin embargo, si sobreviven, pueden ayudar a que el ecosistema se recupere despuŽs de una tormenta filtrando el exceso de sedimento del agua salada. ! INTRODUCTION Increased incidences of extreme weather events especially precipitation extremes have been linked to human influences on climate (Coumou & Rahmstorf, 2012) . Extreme precipitation events can create drastic salinity changes in marine ecosystems (Cheng, Chang, Deck, & Ferner, 2016) . Most marine org anisms cannot maintain osmoregulation in freshwater . Bivalve survival is threatened by salinity changes (Cheng et al., 2016) . B ivalve s such as oysters and mussels are filter feeding marine invertebra tes with a soft body contained inside a hinged shell (Ruppert, Edward E.; ! Fox, Richard S.; ! Barnes, 2004) . These creatures feed on suspended organic matter by filtering seawater through their gills , selecting particles for food to be digested , and rejecting other particles to be expelled as mucus bound feces or ps e udofe ces (Iglesias et al. 1998) . Small particles such as silt, which pass through a bivalve's body, are taken out of the water and deposited at the ocean bottom increasing water clarity ( Ecosystem Concepts for Sustainable Bivalve Mariculture , 2010) . This water filtration p rovide s important ecosystem services that can help to offset anthropogenic pollution and other human induced ecosys tem imbalances. Oyster and mussels can reduce seawater turbidity when they remove inorganic particles from suspension counteracting sedimentation from erosion into waterways . This increases light avai lability essential for primary production including incr eased sea grass productivity (Peterson & Heck, 1999) . Bivalves can also remove anthrop ogenic nitrogen pollution from a ffected waterways (Carmichael, Walton, & Clark, 2012) . Additionally, they sequester carbon for shell building helping to counteract human induced ocean acidificat ion (Filgueira et al., 2015) . Bivalve shells are also substr ate that creates habitat for fou ling communities (Coen & Grizzle, 2007) . Bivalves naturally improve the health of wild ecosystems and support the growth of many other marine organisms . Bivalves are being used as a key component in restoration proj ects aimed to clean up areas hea vily impacted by humans . Bivalves are used in fish mariculture systems . They offset pollution caused by fish feces that results in excessive phosphorus, carbon, and nitrogen inputs in waterways (Wu, 1995) . Sustainable maricult ure projects are becoming an increasingly important alternative to traditional fishing methods because of the devastating effects of overfishing on coastal ecosystems (Jackson et al., 2001) . At my study site in Bahia Tomas near Cuajiniquil Costa Rica, Frank Joyce maintain s a fish mariculture project which he hopes can help be an alternative to over fishing the area. These nets create an artificial habitat

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Tropical Bivalves in Extreme Storms Hudson $ ! for bivalve s to grow, congregate, and filter the water. The most common of bivalve mollusks that can be found on the nets are my study species: Pinctada m azatlanica , Pteria sterna , and Modiolus cap ax . Although these species can act to mitigate some anthropogenic effects on coastal ecosystems, extreme i mbalances threaten some individuals of my study species in some situations . In October 2017 , Tropical Storm Nate hit Costa Rica causing widespread destruction and casualties. F reshwater flooded the Rio MurciÂŽlago , which drains into Bahia Tomas . The mariculture employees stated that the bay was entirely flooded with freshwater and silt deposits substantiall y lowering the salinity of the bay. Although bivalve s are tolerant to many extremes, little is known about the capacity of Pinctada mazatlanica, Pteria sterna , and Modiolus capa x adults to tolerate salinity changes. In my study, I addressed the question: How are survivorship and filtration rates of Pinctada mazatlanica , Pteria sterna , and Modiolus capax affected by salinity changes? METHODS I collected my data near Cuajiniquil, a small fishing village on the Northern Pacific Coast of Costa Rica from 12 M ay to 18 May 2019 . I collected my specimens in Bahia Thomas from a Mariculture project maint ained by Frank Joyce. T o study bivalves' response to salinity change , I exposed nine replicates of Pinctada mazatlanica , Pteria sterna , and Modiolus capax ! to 0%, 2%, and 4% salinity. I tested for water f iltration ability, and survivorship using the following methods: ! Set up T o create my fresh and brackish water treatments, I collected 135 liters of fresh water from the Rio MurciÂŽlago and transported it to my study site in large jugs . The mariculture employees , Tono Castro , Juan Carlos Castro , and Freddy Ampie helped me free dive to collect the species Pinctada mazatlanica , Pteria sterna , and Modiolus capax ! from the mariculture nets. I measured the height, width, an d circumference of each individual . I then filled nine buckets with 5L of ambient salt water from Bahia Thomas (4% Salini ty). Then filled an additional nine buckets with 2.5L of ambient salt water and 2.5L of freshwater from Rio MurciÂŽlag o (2% Salinity). Then I collected one extra bucket with ambient water as a control and to determine settlement rate. I used a refractometer to check the salinity of the water in my buckets. They remained at 4%(Salt), 2% (Brackish), and 0% (Fresh) for the 4 8 hours of my experiment (Table 1) . ! Survi v orship I exposed three individuals of each species to three different salinities (4%, 2% , 0 %) for 48 hours and recorded survivorship at three time points: 4 hours, 24 hours, and 48 hours . I determined if the bivalves were still alive by observing if the shell was open or closed. If the shell was open , I would perturb the bivalve. I f the individual closed its shell, I considered it " alive ." If the shell remained open after disturbance including dropping the in dividual into the bucket, I considered it " dead. " If the shell remained closed, I picked up the individual and tried to gently open its shell, which would remain firmly shut if still alive and fall open if dead . After 48 hours, I repeated the experiment wi th new individuals and new water for a total of 81 individuals across all salinities and species. !

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Tropical Bivalves in Extreme Storms Hudson % ! ! Filtration Rates ! After placing the individuals in buckets, I allowed them to acclimate for at least 30 minutes. I then added 20 ml of silt to each bucket collected from the ocean floor underneath the mariculture nets. The mariculture employees stated that Tropical Storm Nate deposited this silt on the ocean floor in 2017. I used the silt to increase th e turbidity of th e water in the buckets to measure the bivalve's ability to filter the silt out of the water. I used a protractor with fine equally distanced marks pressed agents the side of the bucket parallel to the bottom as well as a measuring tape up the side of the bucket to act as a precise small scale Secchi Disk. I measured the number of centimeters into the water that I could still distinguish the marks on the protractor. I measured the water turbidity with this method just after I placed the mu d into the bucket, and after about 1 hour for each bucket. Because filtration time slightly varied between each bucket, I calculated clearance rate based on the difference in water clarity divided by the number of minutes after the silt was added . In addit ion , I measured the clarity difference in one hour for the control bucket to determine the settlement rate of the silt in the water. I differentiated the increase in water clarity due to settlement with the increased clarity due to bivalve filtration. When calculating final filtration rate, I subtracted the settlement rate from the total clearance rate to calculate the filtration rates. I repeated all steps 3 times for a total 81 individuals across all salinities and species . Table 1: Diagram of Experimental Treatments Salinity : Species : 0% 2% 4% Pinctada m azatlanica 3 trials 3 individuals= 9x (# of individuals and buckets) 3 trials 3 individuals= 9x 3 trials 3 individuals= 9x Modiolus capax 3 trials 3 individuals= 9x 3 trials 3 individuals= 9x 3 trials 3 individuals= 9x Pteria sterna 3 trials 3 individuals= 9x 3 trials 3 individuals= 9x 3 trials 3 individuals= 9x Data Collected Filtration Rates Morality after 6, 24 and 48 hours Control Bucket for Silt Settlement rate Total= 81 individuals

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Tropical Bivalves in Extreme Storms Hudson & ! Study Species Pteria sterna , Pinctada mazatlanica , and Modiolus capax identified with a bivalve seashell guidebook (Coan, Valentich Scott, & Bernard, 2000) . Yolanda Camacho confirmed my identification of Modiolus capax . Pteria sterna Pinctada mazatlanica Modiolus capax

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Tropical Bivalves in Extreme Storms Hudson ' ! RESULTS Bivalve species differed from each other with respect to survivorship and filtration rate depending on salinity. Survivorship based on Salinity at 24 Hours Salinity treatments caused significant differences in survivorship for Pteria sterna at 24 hours (X 2 = 34.37 p < .0001) . I did not find significant differences between salinity treatments for Pinctada mazatlanica or Modiolus capax after 24 hours. I n salt water, 100% of all 3 species survived. In brackish and fresh water, none of the Pteria sterna survived until 24 hours . In brackish water, Modiolus capax and Pinctada mazatlanica survived less tha n in saltwater at 87.5% and 66.6% respectively . Additionally , in freshwater, Pinctada mazatlanica survivorship was the same as in brackish water and Modiolus capax was slightly higher with 100% survivorship. Figure 1: Species survivorship in salt, brackish, and freshwater after 24 hours.

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Tropical Bivalves in Extreme Storms Hudson ( ! Survivorship based on Salinity at 48 Hours Salinity treatments caused significant differences in survivorship at 48 hours for Pinctada mazatlanica and Modiolus capax ( X 2 = 7.415, p = 0.0245 and X 2 = 8.927, p = 0.0115) . I did not find a significant difference between salinity treatments for Pteria sterna . At 48 hours, Pteria sterna had 11.11% survivorship in saltwater and 0% survivorship in brackish and freshwater. Modiolus capax had 100% survivorship in saltwater, 75% in brackish water, and 44.44% in freshwater. Pinctada mazatlanica had intermedia te survivorship with 66.66% in saltwater, 22.22% in brackish, and 11.11% in freshwater. Freshwater cause d the highest mortality for all three species. Figure 2 : Species survivorship in salt, brackish, and freshwater after 48 hours. Survivorship based on Species Pteria s terna had significantly lower survivorship then both Pinctada m azatlanica and Modiolus capax at 48 hours across all salinities. In contrast, Modiolus capax showed

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Tropical Bivalves in Extreme Storms Hudson ) ! significantly higher survivorship at 48 hours then Pteria s terna and Pinctada m azatlanica ( Figure 1, ANOVA F= 6.18 , P= 0.011). Species Filtration Rates in Salinity Changes P teria sterna , Pinctada mazatlanica , and Modiolus capax had positive filtration rates in salt water indicating an ability to filter silt from saltwater (Figures 3,4,5 ) . All species had significantly lower filtration rates in fresh and brackish water (F igures 3 , 4,5 ANOVA Pteria sterna : ! *+!,!-..."!/+!#'-&0 1! Pinctada mazatlanica : *+!,-..."!!/+! %'-''%& ! Modiolus capax : *+ !,-..."!/+!$(-%)0$ ! ) . Negative filtration rates showed a decrease in water quality compared to the control bucket containing no oysters or mussels. This is likely due to death of marine organisms living on the bivalve shell which decreased water clarity. Figure 3: Pteria sterna filtration rate in Fresh (0%), Brackish (2%), and Salt (4%). n= 9 for each treatment P= < .0001 F= 26.59 X axis shows the probability density of the filtration rate.

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Tropical Bivalves in Extreme Storms Hudson 0 ! Figure 4: Pinctada mazatlanica filtration rate in Fresh (0%), Brackish (2%), and Salt (4%). n= 9 for each treatment , P= <.0001 , F= 46.6645 . X axis shows the probability density of the filtration rate. Figure 5: Modiolus capax filtration rate in Fresh (0%), Brackish (2%), and Sal t (4%). n= 9 for each treatment, P= <.0001, F= 37.4893 . X axis shows the probability density of the filtration rate.

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Tropical Bivalves in Extreme Storms Hudson ". ! DI SCUS S ION Salinity treatment had a significant effect on survivorship (Figure 1,2). Salinity had a significant effect on Pteria sterna after only 24 hours as most of the individuals in saltwater survived, while those in brackish and freshwater died . Pteria sterna died the fastest acro ss all treatments suggesting a lower ability to tolerate stressful events. Pteria sterna is a non nativ e oyster to Bahia Tomas which is less tolerant to low salinities then the native species , Pinctada mazatlanica , and Modiolus capax. Significant differences between the salinity treatments could be observed at 48 hours for Modiolus capax , and Pinctada mazatlanica . Modiolus capax was the most tolerant to low salinities and also the only mussel (Table 2) . Although each of these three species was found growing together in large numbers at my study site, they each have their own individual tolerances to fresh and brackish water. Based on these results, it seems that Pteria sterna could not survive 24 hours in a Tropical storm if salinities reached below 2%. Most individuals of Pinctada mazatlanica , and Modiolus capax survive d 24 hours in salinities below 2%. However , many Pinctada mazatlanica individuals die d between 24 and 48 hours of exposure to salinities below 2%. Most Modiolus capax individuals could survive for 48 hours at 2% salinity or above, but in 0% salinity, abo ut half of the individuals die d . If the Bahia Tomas was completely flooded with freshwater during Tropical Storm Nate , such that the salinity dropped below 2% for longer tha n 48 ho urs, it is likely that almost all my species died in the storm. If the storm was less severe and a salinity less the n 2% was maintained for less tha n 24 hours, then many Pinctada mazatlanica , and Modiolus capax could have survived . As climate change continues to worsen the severity of tropical storms, it will be more and more difficult for bivalves to survive (Easterling et al., 2000) . My results corroborate the idea that salinity changes are a major reason for mortality of bivalves after storms (Cheng et al., 2016) . Differences in species survivorships could be attributed to each species' life history (Table 2). Although Pteria sterna was reported as intertidal to 25m, Minor Lara, a local diver and naturalist reported that Pteria sterna could be found growing on Black Coral at depths 50 100 meters (Bo et al., 2009) . Pteria sterna seems to be better adapted to the deep ocean with very little threat of salinity change. Modiolus capax however can be found growing in the mangroves of Cuajiniquil at the outlet of the Rio MurciÂŽlago , which experiences extreme fluctuations in salinity. Modiolus capax appears to be better adapted to an environment with lower salinities. In addition, Modiolus capax has siphons that it uses to take in water without having to open the entire shell (Dinesen & Morton, 2014) . This could allow this mussel to be more able to tolerate hypo osmotic stress . Hypo osmotic stress occurs when salt concentrati on inside a cell is greater tha n outside. As a result, water flows into the cell membrane, which results in cell volume expansi on until the cell wall breaks (Lane & Pekny, 2004) . Hypo osmotic stress can result in mortality among many marine invertebrates (Pierce, 1982) . When bivalves are transferre d directly to a low salinities, they react by closing their shells (Hoyaux, Gilles, & Jeuniaux, 1976) . I observed this behavior in most of my indiv iduals upon placing them in fresh and brackish water. Mortality could have resulted from hypo osmotic stress, and /or a lack of oxygen. Bivalves consume oxygen by filtering water through their gills (Vahl, 1972) . When they close their shells as a reaction to decreased salinity, they may not be able to get the oxygen they nee d. My data on filtration rates exemplify this shell closing response to a decreased salinity.

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Tropical Bivalves in Extreme Storms Hudson "" ! Filtration rates of Pteria sterna , Pinctada mazatlanica , and Modiolus capax are below zero and significantly lower in brackish and freshwater then in saltwater (Figures 3,4,5). This suggests that these species can filter silt out of seawater, however they will not filter in lower salinities (2% and below) . The shell closing behav ior I observed in fresh and brackish water could explain this. They may not be filtering because they are attempting to protect themselves from hypo osmotic stress. In saltwater however, t hese species can help the ecosystem recover after a storm by filteri ng silt out of the water increasing the amount of light that can penetrate to other organisms that rely on light (Peterson & Heck, 1999) . If these species are to be used for restoration however, careful consideration should be put on the placement of these sessile bivalves. For example, avoiding marine areas that may experience large influxes of freshwater, such as close to a river mouth, ca n keep conservationists and oyster farmers from experiencing mass mortality and losing a lot of money. Oyster or mussel far mers could move their species away from the mouth of a river in extreme storms. They could also sink down oysters lower into the water column to avoid the layer of freshwater that forms on the ocean surface in extreme precipitation events. They may even be able to ta ke their species out of the water if there is a threat of a storm. Oyster farmers in Australia take their oysters out of water for up to two weeks (United States. National Marine Fisheries Service., n.d.) . Although the survival time out of water varies by species, it could be an alternative to massive die offs due to freshwater. Knowledge of each species ' salinity toleranc es and filtration rates can help oyster and mussel farmers keep their farms profitable and conservationists to properly use this biological tool. Table 2: Species Descriptions (Coan et al., 2000) , (Dinesen & Morton, 2014) Species Pter ia sterna Pinctada mazatlanica Modiolus capax Common name Pacific wing o yster Mazatlan pearl oyster Horse Mussel Range Goleta California (34.4 ¡ N) to Peru 11.8¡S) Sonora (29.0 ¡N ) to Peru (5.1 ¡ S) Pacific Grove, CA (36.6 ¡ N) to Lambayeque (6.5 ¡ S) Habitat Intertidal Zone to 25m Intertidal Zone to 25m Intertidal zone 35m Unique Characteristics Internal Fertilization Internal Fertilization External fertilization Siphon ACKNOWLEDGEMENTS There should be many co authors on this paper because of the number of people who helped me with this project. I am forever grateful for Frank Joyce for his, humor, list making tips, help with collecting 135 liters of fresh water, willingness to drive back to Minors house to get my mask and fins, and limitless mentorship that made this project happen. Thank you to Richard for spending over 20 hours ou t on the boat helping me collect data. You made my life SO much easier. Thank Juliet Cohen for inspiring me with your project and ideas on bivalve filtration. I would not have been able to figure this out without you. Thank you to Juan Carlos , Tono, and Fr eddy for helping me with all things

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Tropical Bivalves in Extreme Storms Hudson "# ! mariculture. Thanks , Tono for the pineapple when I forgot my lunch. Thank you to Victor for letting me borrow his yacht. Thank you Minor and I vania Lara for dr i ving me out to the mariculture site and always keeping the e nergy light and comico. Thank you to Yolanda Camacho for confirming my identification of Modiolus capax . Thank you to ! Emilia Triana for helping try to understand statistics and mentoring me. Lastly, thank you to m y Cuajini quil buddies for making those two weeks some of the very best times in the program. LITERATURE CITED Bo, M., Bavestrello, G., Canese, S., Giusti, M., Salvati, E., Angiolillo, M., & Greco, S. (2009). Characteristics of a black coral meadow in the twilight zone of the central Mediterranean Sea. Marine Ecology Progress Series , 397 , 53 Ð 61. https://doi.org/10.3354/meps08185 Carmichael, R. H., Walton, W., & Clark, H. (2012). Bivalve enhan ced nitrogen removal from coastal estuaries. Canadian Journal of Fisheries and Aquatic Sciences , 69 (7), 1131 Ð 1149. https://doi.org/10.1139/f2012 057 Cheng, B. S., Chang, A. L., Deck, A., & Ferner, M. C. (2016). Atmospheric rivers and the mass mortality of wild oysters: insight into an extreme future? Proceedings of the Royal Society B: Biological Sciences , 283 (1844), 20161462. https://doi.org/10.1098/rspb.2016.1462 Coan, E. V., Valentich Sc ott, P., & Bernard, F. R. (2000). Bivalve seashells of western North America ! : marine bivalve mollusks from Arctic Alaska to Baja California . Santa Barbara Museum of Natural History. Retrieved from https://www.researchgate.net/publication/256082162_Bivalve _Seashells_of_Wester n_North_America_Marine_Mollusks_from_Arctic_Alaska_to_Baja_California Coen, L. D., & Grizzle, R. E. (2007). The importance of habitat created by molluscan shellfish to managed species along the Atlantic Coast of the United States . Retri eved from https://www.researchgate.net/publication/285046037 Coumou, D., & Rahmstorf, S. (2012). A decade of weather extremes. Nature Climate Change , 2 (7), 491 Ð 496. https://doi.org/10.1038/nclimate1452 Dinesen, G. E., & Morton, B. (2014). Review of the fun ctional morphology, biology and perturbation impacts on the boreal, habitat forming horse mussel Modiolus modiolus (Bivalvia: Mytilidae: Modiolinae). Marine Biology Research , 10 (9), 845 Ð 870. https://doi.org/10.1080/17451000.2013.866250 Easterling, D. R., E vans, J. L., Groisman, P. Y., Karl, T. R., Kunkel, K. E., Ambenje, P., É Ambenje, P. (2000). Observed Variability and Trends in Extreme Climate Events: A Brief Review * . Bulletin of the American Meteorological Society , 81 (3), 417 Ð 425. https://doi.org/10.11 75/1520 0477(2000)081<0417:OVATIE>2.3.CO;2 Ecosystem Concepts for Sustainable Bivalve Mariculture . (2010). Washington, D.C.: National Academies Press. https://doi.org/10.17226/12802 Filgueira, R., Byron, C., Comeau, L., Costa Pierce, B., Cranford, P., Ferr eira, J., É Strohmeier, T. (2015). An integrated ecosystem approach for assessing the potential role of cultivated bivalve shells as part of the carbon trading system. Marine Ecology Progress Series , 518 , 281 Ð 287. https://doi.org/10.3354/meps11048 Hoyaux, J., Gilles, R., & Jeuniaux, C. (1976). Osmoregulation in molluscs of the intertidal zone. Comparative Biochemistry and Physiology Part A: Physiology ,

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Tropical Bivalves in Extreme Storms Hudson "$ ! 53 (4), 361 Ð 365. https://doi.org/10.1016/S0300 9629(76)80157 0 Jackson, J. B., Kirby, M. X., Berger , W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., É Warner, R. R. (2001). Historical overfishing and the recent collapse of coastal ecosystems. Science (New York, N.Y.) , 293 (5530), 629 Ð 637. https://doi.org/10.1126/science.1059199 Lane, E. B., & Pe kny, M. (2004). Stress Models for the Study of Intermediate Filament Function. Methods in Cell Biology , 78 , 229 Ð 264. https://doi.org/10.1016/S0091 679X(04)78009 7 Peterson, B. J., & Heck, K. L. (1999). The potential for suspension feeding bivalves to incre ase seagrass productivity. Journal of Experimental Marine Biology and Ecology , 240 (1), 37 Ð 52. https://doi.org/10.1016/S0022 0981(99)00040 4 PIERCE, S. K. (1982). INVERTEBRATE CELL VOLUME CONTROL MECHANISMS: A COORDINATED USE OF INTRACELLULAR AMINO ACIDS AN D INORGANIC IONS AS OSMOTIC SOLUTE. The Biological Bulletin , 163 (3), 405 Ð 419. https://doi.org/10.2307/1541452 Prog, S., Kisrboe, T., & Mshlenberg, F. (1981). MARINE ECOLOGY PROGRESS SERIES Particle Selection in Suspension Feeding Bivalves (Vol. 5). Retriev ed from https://www.int res.com/articles/meps/5/m005p291.pdf Ruppert, Edward E.; ! Fox, Richard S.; ! Barnes, R. D. (2004). Invertebrate zoology: a functional evolutionary approach . Systematic Biology . https://doi.org/10.1080/10635150490472977 United States. National Marine Fisheries Service. (n.d.). Marine Fisheries Review. Retrieved from http://aquaticcommons.org/9751/ Vahl, O. (1972). Porosity of the gill, oxygen consumption and pumping rate in Cardium edule (L.) (Bivalvia). Ophelia , 10 (2), 109 Ð 118. https: //doi.org/10.1080/00785326.1972.10430107 Wu, R. S. S. (1995). The environmental impact of marine fish culture: Towards a sustainable future. Marine Pollution Bulletin , 31 (4 Ð 12), 159 Ð 166. https://doi.org/10.1016/0025 326X(95)00100 2


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