![7
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Bodkin, J.L., 1986. Fish assemblages in
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off central California. Fishery Bulletin,
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Zygoptera) as paratenic hosts in the
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Marine Parasitology, pp.123–169.
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Creek in western Nebraska. The Journal
of parasitology, 89(2), pp.346–350.
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adaptation to locally common host
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Want to Know about the Fishes of the
Pacific Coast: A Postmodern
Experience. Santa Barbara: Really Big
Press.
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and trends in the molecular systematics of
anisakid nematodes, with implications for
their evolutionary ecology and host-
parasite co-evolutionary processes.
Advances in parasitology, 66, pp.47–148.
Available at:
http://www.sciencedirect.com/science/art
icle/pii/S0065308X08002029 [Accessed
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species of flukes (Digenea: Bucephalidae:
Prosorhynchinae) from the western
moray gymnothorax woodwardi
(Anguilliformes: Muraenidae) from off
Western Australia, with replacement of
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Roberts, L. S., Janovy, J., & Nadler, S. (2013).
Gerald D. Schmidt and Larry S.](https://image.slidesharecdn.com/2133e4f7-0dba-4eb9-82fe-161d240820d1-170125032515/85/Final-Paper-Adolfo-7-320.jpg)
Final Paper - Adolfo
- 1. 1 Diverse Parasites of the Señorita Wrasse (Oxyjulis californica) in the Santa Barbara Kelp Forests Adolfo Hernandez, Dana Morton Zoology, Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara ABSTRACT: Parasitic interactions play a large ecological role, but are unaccounted for in most food webs. In systems where parasites have been examined, parasites are usually most diverse in common hosts that are central in food webs. In the Santa Barbara kelp forests, the Señorita Wrasse (Oxyjulis californica) fills this role. Despite its abundance, there are no published records of endo- parasites for this fish. The objective of this study was to identify parasites using O. californica as a host, and use this data to inform construction of a more accurate kelp forest food web. O. californica were collected by trained divers by spear at two different kelp forests off the coast of Santa Barbara. I conducted a full parasitological assessment. Based off of the types of parasites found and published information on the diet of the fish, we created a list of possible predators/prey of O. californica. A total of 12 fish were dissected and 7 parasite groups were found. Three species of nematodes (Nematoda) had the highest frequency and were abundant in liver and stomach tissues. Larval tapeworms (Cestoda) were found in intestinal tissues along with fluke (Trematoda) cysts which were also located externally at the base of the fins. A single adult fluke was found in the body cavity presumably located in the urinary bladder. Spiny-headed worm (Acanthocephala) cysts were found in liver and stomach tissues. A few crustacean groups (Copepoda, Isopoda, Amphipoda) were attached externally. Associations were used to create links in the food web between predator/prey interactions. INTRODUCTION Parasitic interactions may play a large ecological role, but are unaccounted for in most food webs (Arias-González & Morand 2006). The complex lifecycle of parasites in which multiple hosts are infected throughout the course of the parasite’s lifecycle (Auld & Tinsley 2014), can act as bioindicators for free- living communities and help establish predator/prey interactions (Hechinger et al. 2007). To observe specific organisms in their natural setting and assess gut content samples can be time consuming and inefficient. Parasitic associations can be used to determine relationships between host diet and trophic transmission of parasites (Williams et al. 1992). Some parasitic interactions are host species specific and only provide answers to directed questions on the organism of study. For the purpose of these studies it is important to focus on hosts common to the environment and have a diverse ecological role, in order to provide more general information that can be applied across different areas of interest. In systems where parasites have been examined, parasites are usually most diverse in common hosts that are central in food webs (Lively & Dybdahl 2000). The Señorita wrasse (Oxyjulis californica) is found along the coast of California and is common within the kelp forest habitat (Bodkin 1986). As a secondary consumer in the food web, it acts as both predator and prey which allows parasites to treat it as an intermediate host (Love, 2011). Its diet consists of small invertebrate organisms such as copepods, isopods and bacteria as well
- 2. 2 as free-living invertebrates such as polychaetes, crustaceans and mollusks (Hobson 1971). Due to its generalist diet, O. californica may be exposed to trophically transmitted parasites at regular periods and may be an important host in a parasitic lifecycle. The objective of this study was to identify and characterize the metazoan parasites of O. californica. The list of parasites associated with O. californica was used to identify links between predator and prey interactions used for transmission of parasites from one host to another. MATERIALS AND METHODS O. californica were collected off the coast of Santa Barbara, California, at two different sites: Arroyo Burro and Mohawk Reef. The fish used in this study were collected by certified AAUS SCUBA divers using spears. After the fish were captured, the fish were put into individual plastic bags, immediately placed on ice, and dissected within 72 hours. Fish that were not to be dissected within the 72 hour period were stored in a – 21°C freezer until dissection. At the time of dissection, each fish was weighed and total and standard lengths were measured. Before each individual was dissected, a search for any external parasites was conducted; this included thorough inspection of the plastic bag the fish were stored in. Once dissected, individual tissue types were pressed thin between two glass “squash plates” and examined using a stereo microscope. For most organs, the entire organ was squashed (liver, spleen, brain, heart, digestive tract). For tissues that are bilaterally symmetric, a side (left or right) of the fish was chosen at random at the beginning of each dissection and was used to subsample those tissues (e.g. pectoral fin, pelvic fin, gill, eye, gonad, kidney). Very large tissues (e.g. muscle), a sub-sample was weighed. All parasites were recorded, examined under higher magnification using a compound microscope, and identified to the lowest level possible. For many larval stages, identification to species is not possible, so “morpho-species” were assigned names. For every new parasite species detected, pictures and voucher samples were taken. Percent prevalence and intensity were calculated for each parasite species. RESULTS A total of 17 parasite species pertaining to 7 taxonomic groups were found in O. californica: 3 of which are ecto- (Copepoda, Amphipoda, Isopoda) and 4 endo-parasites (Nematoda, Trematoda, Cestoda, Acanthocephala). The nematodes had the highest prevalence (# of host infected/total host observed) and mean intensity (mean # of individuals/host), followed by the trematodes, cestodes, and acanthocephalans (Graph 1). All parasites were found as larval forms, except for the ecto-parasites and a single adult trematode from the urinary bladder of the host. Nematodes were the most prevalent parasite found (Graph 1) and had the highest mean and maximum intensity (10 and 19, respectively) among the other groups of parasites. Present in various tissue types, they were most abundant in liver and stomach tissues (Graph 2) in which they were either found in sheaths or encysted. 3 distinct morpho-species were identified. Out of the 3 species Nematode A was the most prevalent found in all 12 fish and varied most in tissue types (gonad, intestine, kidney, liver, spleen, stomach, swim bladder). Nematode C (intestine) and Nematode B (liver, spleen, stomach) never co-occurred in the same host and were more confined to certain tissue types (Graph 1).
- 3. 3 Graph 1 (RIGHT). Percent prevalence is shown for each parasite group found associated with O. californica. Each letter represents a separate species corresponding to that group, were species can occur independently from others or within the presence of another. Graph 2 (ABOVE). Tissue parasite count is shown for all tissues dissected. Graph was formatted in order to be viewed more efficiently. Bars touching the border of the graph have indicating number (eg. liver: nematode, 65).
- 4. 4 Trematodes were second most prevalent (0.8333) with a mean intensity of 2.5 (maximum = 11). Most trematodes were found encysted as metacercaria (a larval stage). Metacercaria were sometimes found in heart tissue but were most common at the base of the fins (Graph 2). There were 5 distinct species, 2 of which were identified to genus: D = Dolfustrema, and E = Phyllodistomum. Dolfustrema (D) was present in 7 of the 12 fish dissected, and was found at the base of fins (pectoral, caudal, anal) and sometimes fillet muscle and stomach mesentary. Phyllodistomum (E) was the only adult endo- parasite observed and was found in the coelom when the swim bladder was being examined, but was presumably from the urinary bladder which had ruptured. Both Trematode H and Trematode E were located in heart tissue with a single instance of them being found in the liver. Trematode G was only found in heart tissue and never co-occurred with either of the other species. Trematode E and Trematode H occurred only along with Trematode D (Graph 1). Tapeworms had a prevalence of 0.5833 and a mean intensity of 3 (maximum = 6). They were most abundant in stomach and intestinal tissues (Graph 2) and were found in their larval plerocercoid stage. A total of 3 species were found; 1 belonging to the Order Tetraphyllidea and 2 to the Order Trypanorhyncha. Cestode I was present in 5 of the fish and most abundant in intestinal tissues with a few occurrences in stomach tissues. Cestode J was found in liver tissue and Cestode K was found in stomach and intestine tissues. None of the species co-occurred with one another (Graph 1). Acanthocephalans had a prevalence of 0.3333 and a mean intensity of 3.25 (maximum = 7). They were most abundant in liver and stomach tissues (Graph 2) and were found encysted as cystacanths. Only 2 species were found: Acanthocephalan L and Acanthocephalan M. With a prevalence of 0.25, Acanthocephalan M was most abundant in liver and stomach tissues, and found in other tissues (gonad, intestine). Acanthocephalan L was found in liver and stomach tissues. There was a single instance in which both species co- occurred with one another (Graph 1). Three groups of ecto-parasites were found (Graph 2): Copepoda, Amphipoda, Isopoda. 2 species of copepods were found. They had same prevalence values and co- occurred in one instance (Graph 1). Copepod N was found attached externally and Copepod O was found attached to the gill filaments. 1 species of amphipod was found attached to the pectoral fin, and 1 species of isopod (a Gnathiid) was found on the body surface. DISCUSSION With the exception of the single adult trematode, all endo-parasites were found as larvae. These larvae compromised the majority of parasitic interactions observed in O. californica. This indicates that most of the parasites we observed use O. californica as an intermediate host, most likely due to its role as a secondary consumer in the kelp forest habitat (Love, 2011). From the 7 parasitic groups found associated with O. californica, 4 groups (Nematoda, Trematoda, Cestoda, Acanthocephala) contained parasites which are trophically transmitted. Their identification allows general predator/prey interactions to be established between O. californica and other hosts needed by the parasite’s lifecycle. Nematoda All nematodes were either found in sheaths or encysted in the fish’s tissues (rather than in the intestinal lumen); an indicator for the continued development towards the sexual adult stage (Priess & Hirsh 1986). The
- 5. 5 presence of juvenile nematodes enforces the statement that O. californica acts as an intermediate host in order for parasites to move from the bottom to the top of the kelp forest food web. From the 3 nematode species observed, Nematode A is believed to belong to the Anasakis or Contracecum genera. Belonging to the Anisakidae family both have related parasitic lifecycles utilizing similar animals as intermediate and definitive hosts. These nematodes infect a crustacean, possibly a copepod, amphipod, isopod, etc, and use it as their first intermediate host. O. californica appears to be used as an additional intermediate host, but other paratenic hosts may also be used. Anasakis and Contracecum use mammals as definitive hosts, so possible final hosts in this system include harbor seals, California sea lions, and dolphins (Mattiucci & Nascetti 2008). Trematoda With the exception of the single adult, all trematodes were observed in their larval stage encysted in tissues as metacercaria. In the general trematode lifecycle, the first intermediate host is a mollusk which produces cercaria larvae. For some species, cercaria directly infect the definitive host (always a vertebrate), but in other species the cercaria infects a secondary intermediate host. This second intermediate host must be consumed by the definitive host for the life cycle to be completed (Roberts, et al., 2013). Here, O. californica appears to act as a secondary intermediate host (Bolek et al. 2010). From the 5 species of trematodes observed, Trematode D was the most prevalent and identified to the genus Dollfustrema (Bucephalidae). Using a marine snail or bivalve as its primary intermediate host, the cercaria infect O. californica, become metacercaria, and await trophic transmission to the definitive host. Trematodes from the genus Dollfustrema are known to use the California Morey eel as its definitive host (Nolan & Cribb 2010). Trematode E was the only adult endo- parasite found and was identified to the genus Phyllodistomum (Gorgoderidae). Since most research done with this particular genus is limited to descriptions of species, actual host specificity is not well known (Helt et al. 2003), thus details on trophic transmission are not available. Cestoda Cestodes were present in over half of the fish observed. All cestodes were in the plerocercoid larval stage. Cestodes have multiple larval stages, and must be trophically transmitted between each host in the life cycle. Paratenic hosts are often used as well. All cestodes use arthropods as first intermediate hosts, and vertebrates as definitive hosts. Found in the secondary intermediate hosts and being the last cestode larval stage, plerocercoids arose from ingested procercoids: originally developed from oncospheres in the first intermediate host (Roberts, et al., 2013). The two orders of cestode found, Trypanorhyncha and Tetraphyllidea, both utilize similar hosts throughout their lifecycles. Treating small crustaceans (copepods) as first intermediate hosts, O. californica acts as second intermediate host, but it is unclear whether paratenic hosts are used. The diet of O. californica includes copepods, isopods, and amphipods (Hobson 1971), thus the presence of the cestode larvae in this fish indicates that larval stages are also present in the crustacean population. Trypanorhynchs exclusively use elasmobranchs (sharks, skates, rays) as definitive hosts (Olson et al. 2001). Tetraphyllids also use elasmobranchs, but
- 6. 6 some species use other large predator fishes as well. Acanthocephala All individual acanthocephalans were found in their larval cystacanth stage and present in over a third of the fish observed. Although complete lifecycles have been worked out for a small fraction of the known acanthocephalans species, the three major classes (Eoacanthocephala, Palaeacanthocephala, Archiacanthocephala) follow similar host transmission patterns (Roberts, et al., 2013). Requiring only a single intermediate host (a small crustacean: amphipod, isopod), the larval cystacanth is ready to infect the definitive host. In this, case O. californica does not appear to be required to complete the parasite’s lifecycle, but acts as a paratenic host to ensure the survival of the parasite. Infection of O. californica creates a link between small, short-lived intermediate host and the large, long-lived definitive host. As for most larval stages, it was difficult to identify both species found and particular lifecycles were not characterized. In general, it must use an arthropod (likely and amphipod) as its intermediate host, and a vertebrate (mammals, fish, birds) as the definitive host (Wey-Fabrizius et al. 2014). Copepoda, Amphipoda, Isopoda The 3 ecto-parasitic groups (Copepoda, Amphipoda, Isopoda) were all found as adults attached exteriorly to the fish. For the exception of those species that have become highly modified and/or require 2 hosts to complete their lifecycles, lifecycles of the majority of parasitic crustaceans compromise a single host and subsequent pelagic larval stages that lead up to the adult (Boxshall 2005). From the 4 species found (2 copepod, 1 amphipod, 1 isopod), none appeared modified to a large extent except for a single species bearing modified clawed antennae resembling participation in cyclopiform copepod families (Rohde, 2005). No trophic relations were made in these parasites. CONCLUSION We already know O. californica acts as a secondary consumer and is an abundant animal in the kelp forest habitat, an ideal organism for parasites to use as an intermediate or paratenic host. The present study shows that parasites do indeed treat O. californica as an intermediate host due to the fact that most parasitic infections were found in their larval states. Using known parasitic lifecycles from those groups (Nematoda, Trematode, Cestoda, Acanthocephala) most prevalent in the fish, predator/prey relations were made between O. californica and other organisms acting as hosts in the parasites lifecycle. This gave us 4 general lifecycles to work with, which allowed the construction of a more accurate trophic system in the kelp forest food web: providing data on predators (harbor seals, CA sea lions, dolphins, fishes, birds, sharks, eels) and prey (copepods, amphipods, molluscs) that have been identified to be more closely related with O. californica. ACKNOWLEDGEMENTS We thank Dr. Armand Kuris for providing laboratory workspace and the CAMP summer program. This project was partially supported by the LSAMP program of the National Science Foundation under Award no. DMR- 1102531 and by the MRSEC Program of the National Science Foundation under Award No. DMR- 1121053. REFERRENCES Arias-González, J.E. & Morand, S., 2006. Trophic functioning with parasites: A new insight for ecosystem analysis.
- 7. 7 Marine Ecology Progress Series, 320(August 2015), pp.43–53. Auld, S.K. & Tinsley, M.C., 2014. The evolutionary ecology of complex lifecycle parasites: linking phenomena with mechanisms. Heredity, 114(2), pp.125–132. Available at: http://www.nature.com/doifinder/10.103 8/hdy.2014.84. Bodkin, J.L., 1986. Fish assemblages in Macrocystis and Nereocystis kelp forests off central California. Fishery Bulletin, 84(4), pp.799–808. Bolek, M.G., Tracy, H.R. & Janovy, J., 2010. The role of damselflies (Odonata: Zygoptera) as paratenic hosts in the transmission of Halipegus eccentricus (Digenea: Hemiuridae) to anurans. The Journal of parasitology, 96(4), pp.724– 735.Eschmeyer, W. E. (1983). A field guide to Pacific coast fishes of North America. Boston, U.S.A: Houghton Mifflin Company.Hechinger, R.F. et al., 2007. Can parasites be indicators of free- living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia, 151(1), pp.82–92. Boxshall, G., 2005. Crustacean parasites. Marine Parasitology, pp.123–169. Helt, J., Janovy, J. & Ubelaker, J., 2003. Phyllodistomum funduli n. sp. (Trematoda: Gorgoderidae) from Fundulus sciadicus Cope from Cedar Creek in western Nebraska. The Journal of parasitology, 89(2), pp.346–350. Hobson, E.S., 1971. Cleaning symbiosis among California inshore fishes. Fish.Bull.Natl.Oceanic Atmos.Adm., 69(3), pp.491–523. Lively, C.M. & Dybdahl, M.F., 2000. Parasite adaptation to locally common host genotypes. Nature, 405(6787), pp.679– 681. Love, M. S. (2011). Certainly More Than You Want to Know about the Fishes of the Pacific Coast: A Postmodern Experience. Santa Barbara: Really Big Press. Mattiucci, S. & Nascetti, G., 2008. Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host- parasite co-evolutionary processes. Advances in parasitology, 66, pp.47–148. Available at: http://www.sciencedirect.com/science/art icle/pii/S0065308X08002029 [Accessed August 8, 2015]. Nolan, M.J. & Cribb, T.H., 2010. Two new species of flukes (Digenea: Bucephalidae: Prosorhynchinae) from the western moray gymnothorax woodwardi (Anguilliformes: Muraenidae) from off Western Australia, with replacement of the pre-occupied generic name Folliculovarium Gu & Shen, 1983. Systematic Parasitology, 76(2), pp.81– 92. Olson, P.D. et al., 2001. Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular phylogenetics and evolution, 19(3), pp.443–467. Priess, J.R. & Hirsh, D.I., 1986. Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Developmental biology, 117(1), pp.156–173. Roberts, L. S., Janovy, J., & Nadler, S. (2013). Gerald D. Schmidt and Larry S.
- 8. 8 Roberts' Foundations of Parasitology. New York: McGraw-Hill Education. Rohde, K. (2005). Marine Parasitology. Collingwood: CSIRO Publishing. Wey-Fabrizius, A.R. et al., 2014. Transcriptome data reveal syndermatan relationships and suggest the evolution of endoparasitism in acanthocephala via an epizoic stage. PLoS ONE, 9(2). Williams, H.H., MacKenzie, K. & McCarthy, a. M., 1992. Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Reviews in Fish Biology and Fisheries, 2(2), pp.144–176.
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