Global Diversity and Ecological Function of Parasites of Euphausiids

Jaime Gómez-Gutiérrez · So Kawaguchi José Raúl Morales-Ávila Global Diversity and Ecological Function of Parasites of Euphausiids Global Diversity and Ecological Function of Parasites of Euphausiids Jaime Go´mez-Gutie´rrez • So Kawaguchi Jose´ Rau´l Morales-A´ vila

Global Diversity and Ecological Function of Parasites of Euphausiids Jaime Go´mez-Gutie´rrez So Kawaguchi Departamento de Plancton y Australian Antarctic Division Ecologı´a Marina Kingston, Tasmania Centro Interdisciplinario de Ciencias Australia Marinas Instituto Polite´cnico Nacional La Paz, Baja California Sur Mexico

Jose´ Rau´l Morales-A´ vila Departamento de Plancton y Ecologı´a Marina Centro Interdisciplinario de Ciencias Marinas Instituto Polite´cnico Nacional La Paz, Baja California Sur Mexico

ISBN 978-3-319-41053-1 ISBN 978-3-319-41055-5 (eBook) DOI 10.1007/978-3-319-41055-5

Library of Congress Control Number: 2017935492

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This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface

Parasites employ one of the most ubiquitous and specifically diverse trophic strategies on the planet. Marine pelagic organisms provide numerous ecological microhabitats and thus hold many interspecific, parasitic associations. Considering that each host species interacts with multiple parasite species, and also that several parasites can be parasitized themselves (hyperparasitism), the diversity of parasites that infect planktonic and nektonic organisms likely exceeds the diversity of their hosts. This high parasite diversity challenges us to develop a synthesis, partly to understand the density-dependent control they exert on marine populations. We review here the current, worldwide knowledge of parasites interacting with crustaceans of the Order Euphausiacea, showing the complex diversity and life cycles of the parasitic species known so far. The Order Euphausiacea includes 86 species. They usually have broad distributional ranges, and several species form considerably dense social aggregations making large stocks of biomass available for predatory and parasitic interactions. Parasites have co-evolved in multi-specific associations with euphausiid species, affecting eggs and almost all euphausiid life stages (so far, no parasites are known to occur in nauplius, pseudometanauplius or metanauplius larval stages). Thus, parasites tend to be more diverse and prevalent in adult euphausiids than in the larval and juvenile phases. Symbiotic interactions with euphausiid hosts range from apparently innocuous epibionts, through ectoparasites, micropredators, internal parasites and castrators to obligatory histophagous killers (parasitoids). Euphau- siids interact with 18 types of symbionts: (1) pathogenic chitinoclastic bacteria (on the exoskeleton); (2) gut bacteria; (3) fungi, several protists; (4) epibiont diatoms (Bacillariophyta); endoparasitic dinoflagellates, which infect and kill euphausiid eggs, of the Orders (5) Blastodiniales (particularly of the family Chytriodiniaceae) and (6) Syndiniales; (7) Alveolate mesoparasites of the family Ellobiopsidae (like Thalassomyces fagei); (8) epibiont ciliates of the Subclass Suctoria (sessile planktophagous predators); Apostomatida ciliates of the families (9) Foettingeriidae (that feed on the hosts’ moults as exuviotrophic ecto- commensals), (10) Opalinopsidae (attached to the euphausiids mouth appendages);

v vi Preface and (11) Pseudocollinidae (histophagous ciliates); (12) Apicomplexa of the family Gregarinidae (living in gut and hepatopancreas); metazoan endoparasites (13) Trematoda, (14) Cestoda, (15) Nemathelminta and (16) Acanthocephala; and crustaceans (17) isopods of the family Dajidae, and (18) a Rhizocephalan (a single record, likely an accidental infection). Although microsporidians have been reported as endoparasites of krill, it is now clear they were misidentified, confused with apostome ciliates of the genus Pseudocollinia. Thus, microsporidian parasitism has not been confirmed in euphausiids. The discovery of unicellular parasitoids infecting euphausiid eggs (dinoflagellates) and adults (ciliates, Pseudocollinia) challenges the paradigm that predation and starvation are the major sources of euphausiid mortality. The very small size, short life span, high reproductive rates and the now known to be widespread distribution patterns of these parasitoids make them particularly dan- gerous to euphausiid populations. Exuviotrophic ciliates feed on fluids in euphausiid moults, but their roles in setting sinking rates of moults and carbon remineralisation in the pelagic ecosystem are unexplored. They are potentially significant enough to be included in carbon flux numerical models. Pathogenic viral infection has never been studied in euphausiids, but it deserves investigation, because viruses cause lethal infections in decapods and other crustaceans. Also, it is necessary to investigate bacterial diversity and pathogenicity to understand their roles in euphausiid health and population dynamics. Parasitic castrators (Ellobiopsidae, helminth worms, Dajidae) have been recorded from most of the euphausiid species. They typically infect with low prevalence, but current research demonstrates they could be more prevalent than previously thought. Although complete castration does not always occur, the infection can decrease host’s fecundity and fitness. Parasitism is favoured by the dynamic social behaviour and wide trophic spectra of euphausiids. A general perspective is emerging that several parasitic species can influence the dynamics of euphausiid populations, as they do in better-studied top predators. Krill are key intermediate hosts for trophically transmitted helminth parasites, which infect cephalopods, teleost and elasmobranch fish, sea birds and marine mammals. The roles of pathogens and parasites in carbon flux through the marine ecosystem deserve considerably more investigation. Currently, there are records of parasites infecting 49 of the 86 euphausiid species. Euphausiids typically interact with one or maximum two types of epibionts and/or parasites simultaneously in the same individual host. Parasites of the mesopelagic and bathypelagic genera Bentheuphausia, Nematobrachion, Tessarabrachion and Thysanopoda are unknown. The most likely near-future advance in studies of euphausiid’s parasites will be application of molecular methods (particularly multigenomic or metagenomic) to identify and understand the taxonomy, diversity and phylogenetic associations of euphausiid and their parasites. Major concern is focussed currently on several parasites that infect euphausiids as intermediate (nematodes) or final hosts (bacteria), because they may be potential threats to human health. We summarize the potential impacts of these interspecific, symbiotic interactions on the krill life cycle, on their secondary Preface vii productivity and on the biogeochemical cycles of pelagic ecosystems. The lead author dedicates this book to Edward Brinton (1924–2010), Margaret Knight (1925–2014) (Scripps Institution Oceanography) and William T. Peterson (NOAA) for their inspiration and dedication to the study of the taxonomy, biology and ecology of euphausiids in the world oceans. “Nobody likes parasites, but unfortunately they are the majority” J. Go´mez- Gutie´rrez, 2009. Acknowledgements

We thank Professor Charles B. Miller (Oregon State University) and Ira Fogel (CIBNOR) for their English editorial reviews. We thank Springer editors Joao Pildervasser and Susan Westendorf (Springer Science and Business Media) for offering us the great opportunity to contribute to this exciting and significant project, their valuable technical help and infinite patience to complete this book. We thank many parasitology experts for their advice and enthusiastic feedback before and during the writing process of the present literature review: Stephen Landers (Troy University) with exuviotrophic ciliates, Denis Lynn (University of British Columbia) and Michaela Strüder-Kypke (Guelph University) for interaction regarding Pseudocollinia ciliates, Mario Josue´ Aguilar-Meńdez (IPN) for the review of the section on bacteria, and Thomas C. Shirley and Jill Mooney (Uni- versity of Alaska Fairbanks) for discussions on Rhizocephala infecting euphausiids. Special thanks to Professor Frederick G. Hochberg (Department of Invertebrate Zoology, Santa Barbara Museum of Natural History) for his kind generosity and permission to include in this book his unpublished Chromidina nov. sp. ciliate photographs (Fig. 6.12a–e) and for reviewing the Opalinopsidae section of this book. We thank Jorge Arturo del A´ ngel Rodrı´guez for providing us with the data and collaborating with us on Fig. 6.16, whose original data set was published in Go´mez-Gutie´rrez et al. (2015b). We deeply thank Ivań A. Hinojosa-Toledo and Armando Mujica (Universidad Cato´lica del Norte, Chile) and Ivań Castellanos- Osorio (El Colegio de la Frontera Sur, Chetumal) to give us permission to include their photographs of the Dajidae isopod O. bicaulis shown in Fig. 7.10a, b. J.G.-G. thanks Rubeń Escribano, Pamela Hidalgo and Ramiro Riquelme-Bugueno~ (Universidad de Concepcioń, Chile) for their constant support during two research stays at Concepcioń, Chile (2009 and 2010), when we had the opportunity to discover new records of Euphausia mucronata parasites. J.G.-G. deeply thanks Edward Brinton and Annie Townsend (Scripps Institution Oceanography, Univer- sity of California San Diego) for the loan of the euphausiids infested with Dajidae isopods collected in the Pacific Ocean between 1949 and 1964 for taxonomic identification and for having received me for a research stay in 1996 at

ix x Acknowledgements

SIO summarized in Table 7.5. This unpublished information is highly valuable contribution to the section on Dajidae isopods. We thank Carlos J. Robinson (Instituto de Ciencias del Mar y Limnologıá, Universidad Nacional Autońoma de Mexico) for allowing us to participate in multiple oceanographic cruises on board the R/V El Puma (Universidad Nacional Autońoma de Me´xico) in the northwest region of Mexico, where we have been discovering several parasites of subtropical euphausiids, great adventures with a great support and friendship. We thank William T. Peterson (NOAA) for the opportunity to participate on cruises carried out off the Oregon and California coasts (1998–2003) and Dr. Brad Seibel for the oportunity to participate on a cruise on board R/V Oceanus carried out in May 2015 in the central Gulf of California where we took several photographs of Dajidae isopods showed in the present book (Fig. 7.11). We deply thank Kerrie M. Swadling (TAFI, Australia) for allow us to analyze zooplankton samples from an oceanographic cruise carried out along the east coast of Tasmania, Australia in search of parasites of euphausiids. We also thanks to Al Soldner (OSU) and Ariel Cruz- Villacorta (CIBNOR) for their valuable technical support for the Scanning Electron Microscope images showed in Figs. 1.1, 6.6a–e, 6.8e, f, 6.11c, 6.15, 6.16e, 7.8a–g and 8.2f. J.G.-G. thanks Steve Nicol, So Kawaguchi and Robert King for their kind hospitality in Tasmania, Australia, during the initial work on the present book. This review started as part of a sabbatical stay of J.G.-G. at the Australian Antarctic Division (2008-2009) supported by CONACyT (2008–79528) and Centro Interdisciplinario de Ciencias Marinas from Instituto Politećnico Nacional as part of multiple annual and biannual research projects carried out between 2008 and 2016 (SIP-IPN 20080490, 20090090, 20100173, 20110012, 20120948, 20130224, 20140497, 20150113, 20160495). The work benefitted from a CONACyT research project ‘Parasitic interactions of the euphausiids and their predators in the Gulf of California to infer their life cycles’ (CONACyT CB-2012-178615-01). J.G.-G. is supported by an SNI-II fellowship and by the COFAA–IPN and EDI-IPN grants. J. R.M.-A´ . was supported with CONACyT (2012–2015) and BEIFI-IPN PhD grants associated to research projects IPN-SIP 20120948, 20130224, 20140497 and 20150113. We thank Teresa de Jesu´s Barriga Ramı´rez (CICIMAR-IPN librarian) for her valuable help to obtain permissions to use figures from published sources. We acknowledge with thanks the help of the authors, publishers and copyright holders who have agreed to the reproduction of previously published material: Springer Science and Business Media (Fig. 2.1a), Limnology and Oceanography (Fig. 2.3), Journal of Invertebrate Pathology (Fig. 4.1a, b), Springer Science and Business Media (Fig. 4.1c–e), Marine Biology (Fig. 6.1a), G.O. Sars, 1898 (Copy- right Status: Public domain. The Biodiversity Heritage Library considers that this work is no longer under copyright protection) (Fig. 6.2a, b), Journal of Plankton Research (Figs. 6.3a–d and 6.8a, b), Annual Review of Fish Diseases (Fig. 6.4a–e), Journal of the Marine Biological Association of the United Kingdom (Fig. 6.5a), Annie W. Townsend (SIO-UCSD) for allow us to use her photograph showed in Fig. 6.5b,c, Journal of the Oceanographical Society of Japan (Fig. 6.5h), Springer Science and Business Media (Fig. 6.7a–h), Polar Biology, Springer Acknowledgements xi

Science and Business Media (Fig. 6.9), Springer Science and Business Media (Fig. 6.10a–f), F.G. Hochberg (Department of Invertebrate Zoology, Santa Barbara Museum of Natural History) (Fig. 6.12a–e), Diseases of Aquatic Organisms (Fig. 6.13), Protistologica (Fig. 6.17a–d), Parasitology (Fig. 6.18a–f), Polar Biol- ogy, Springer Science and Business Media (Fig. 6.19), Bulletin of the Plankton Society of Japan (Figs. 7.1 and 7.2), Springer Science and Business Media (Fig. 7.3a, b), Parasitology Research (Fig. 7.4), G.O. Sars (Copyright Status: Public domain. The Biodiversity Heritage Library considers that this work is no longer under copyright protection) (Figs. 7.5a, c and 7.9a, c), Journal of Parasitology, Allen Press Inc. (Figs. 7.5b, 7.6c and 7.9b), Zoologische Anzeiger (Copyright Status: Public domain. The Biodiversity Heritage Library considers that this work is no longer under copyright protection) (Figs. 7.5d and 7.6d), Bulletin de l’Institut Oceánographique (Copyright Status: Public domain. The Biodiversity Heritage Library considers that this work is no longer under copyright protection) (Fig. 7.5e), Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening i Kjobenhavn (Copyright Status: Public domain. The Biodiversity Heritage Library considers that this work is no longer under copyright protection) (Figs. 7.5f and 7.6e), International Journal of Parasitology (Figs. 7.5g and 7.6f), Crustacean Research and Dr. Hiroyuki Ariyama (Fig. 7.5h), Cahiers de Biologie Marine (Fig. 7.6a), Journal of Natural History, Taylor & Francis (Fig. 7.6b), Journal of Parasitology (Fig. 7.7a, b, c, e), Ivań A. Hinojosa-Toledo and Armando Mujica (Universidad Cato´lica del Norte, Chile) (Fig. 7.10a), Ivań Castellanos-Osorio (ECOSUR, Chetumal) (Fig. 7.10b), Diseases of Aquatic Organisms with permission of Inter Research (Fig. 7.14), and Journal of Crustacean Biology with permission of Koninklijke Brill NV (Fig. 8.1). Contents

1 Introduction ...... 1 References ...... 10 2 Krill-Parasite Interactions ...... 17 2.1 Krill–Parasite Interaction Is Multispeciﬁc and Highly Complex ...... 17 2.2 Social Behaviour, Parasite Life Cycles, and Infection Mechanisms ...... 25 2.3 Biodiversity and Size Proportion Between Euphausiid and Parasites ...... 32 References ...... 34 3 Viruses ...... 39 References ...... 41 4 Bacteria ...... 43 4.1 Pathogenic and Chitinoclarstic Bacteria ...... 43 4.2 Gut-Symbiotic or Gut-Parasitic Bacteria? ...... 50 References ...... 52 5 Fungi ...... 55 References ...... 56 6 Protista ...... 59 6.1 Bacillariophyta (Chloroepibionts) ...... 59 6.2 Dinoﬂagellata ...... 62 6.2.1 Family Chytriodiniaceae ...... 64 6.2.2 Order Syndiniales ...... 67 6.3 Ellobiopsidae (Mesoparasites) ...... 69 6.4 Ciliophora ...... 81 6.4.1 Suctorida ...... 81 6.4.2 Apostomatida ...... 89

xiii xiv Contents

6.5 Apicomplexa, Eugregarinida ...... 109 6.6 Microsporidia ...... 120 References ...... 121 7 Animalia ...... 133 7.1 Parasitic Worms (Helminths) ...... 133 7.1.1 Trematoda ...... 135 7.1.2 Cestoda (Tapeworms) ...... 138 7.1.3 Nemathelminths (Roundworms) ...... 145 7.1.4 Acanthocephala (Hookworms) ...... 157 7.1.5 Roles of Euphausiid Helminth Parasites in Human Diseases ...... 160 7.2 Crustacea ...... 162 7.2.1 Isopoda (Dajidae) ...... 162 7.2.2 Cirripedia (Rhizocephala) ...... 186 References ...... 187 8 Unknown Parasites and Diseases of Krill ...... 199 References ...... 203 9 Conclusions ...... 207 References ...... 208 Chapter 1 Introduction

Parasitism appeared early in biological evolution as a diverse, ubiquitous, and successful interaction (Lafferty 1999; Lafferty and Kuris 2002). Thus, it is the most common and specifically diverse trophic strategy on the planet. Parasites have evolved remarkably complex life cycles; during their ontogeny, they may interact with multiple and very distinct host species at several trophic levels. Metagenomic analyses indicate parasitism is one of the main symbiotic interactions and most abundant biological component that determine community structure in the global plankton interactome (biological networks; whole set of molecular interactions in a particular cell); explaining a complementary part variability caused by environ- mental and geographic factors (Lima-Mendez et al. 2015). In this book, we review and summarize what is known about this complexity in one group of hosts, the marine planktonic and micronektonic crustaceans of the Order Euphausiacea (“euphausiids”), commonly known as krill. The marine plankton represents a massive (but frequently dispersed) and widespread biomass reservoir that provides numerous ecological microhabitats for interspecific parasitic associations. Considering that each planktonic species can host multiple parasitic forms, and indeed that several parasites are parasitized by other parasites (hyperparasitism), parasitic diversity infecting planktonic and nektonic organisms likely exceeds the diversity of hosts. Lima-Mendez et al. (2015) proposed that all “plankton functional types” are associated with parasites but not always to the same extend. For this review, we selected euphausiids and their epibiont and parasitic diversity because: (1) euphausiids are a taxonomic group with relatively low species diversity (86 species with a well established taxonomic classification into 2 families and 11 genera) compared with other marine crustacean groups (Brinton 1962, 1975; Baker et al. 1990; Brinton et al. 2000); (2) they usually have broad zoogeographic ranges promoting wide distributions of their symbiotic organisms, and so are likely to be studied by scientists from many countries; (3) several krill species attain massive swarms and schools that constitute a large part of the zooplanktonic biomass (Ritz 1994; Verdy and Flierl 2008); (4) they represent a considerable biomass available for multiple predators and parasites,

© Springer International Publishing Switzerland 2017 1 J. Go´mez-Gutie´rrez et al., Global Diversity and Ecological Function of Parasites of Euphausiids, DOI 10.1007/978-3-319-41055-5_1 2 1 Introduction serving as intermediate hosts for trophically transmitted parasites, and (5) their planktonic and micronektonic life phases attain relatively large sizes compared with other planktonic animals, sustaining considerably larger population biomass than other micronektonic organisms (Nicol and Endo 1999; Nicol et al. 2000; Nicol 2003; Brodeur and Yamamura 2005). The relatively large body size of euphausiids facilitates the observation of endoparasites through their naturally transparent exo- skeletons when observed in vivo and by the relatively easy dissection of preserved specimens. Because of their biological and population characteristics, the euphausiids are significant components in the food webs and secondary productivity of marine pelagic ecosystems. Extant euphausiid species likely evolved from a common ancestor some 35–20 million years ago (D’Amato et al. 2008), co-diversifying and interacting with multiple symbionts. Euphausiids have multiple interspecific (symbiotic and parasitic) interactions that likely shape their fitness and natural selection, forming “holobionts”, defined as the host organism plus all of its smaller symbiotic organisms (Rosenberg et al. 2010), or infra-communities (consisting of all parasites of all species found together in one individual host) and the “component community” comprising the sum of all infra-communities (Poulin 2007). Euphausiids have typically a relatively small infracommunity (interacting with less than three types of epibionts and parasites simultaneously) compared with their predators (excluding enteric bacteria that possess a large diversity in each host, Go´mez-Gutie´rrez et al. 2015a); but epibiont exuviotrophic ciliates and parasitoids (Tetraphyllidea Cestoda, Dinoflagellata and Pseudocollinia ciliates) can attain high intensities (Go´mez-Gutie´rrez et al. 2010). Epibionts and parasites of euphausiids are highly diverse, having a broad range of interspecific, accidental, paratenic, intermediate and definitive symbiont-host interactions that range from almost innocuous to deadly (epibiont organisms, pathogens, micropredators, parasites, castrators, and parasitoids) (Fig. 1.1). Although there are attempts to classify such symbiotic interactions (Lafferty and Kuris 2002), frequently there are no clear distinctions among different types of interactions (Bush et al. 2001; Parmentier and Michel 2013). Go´mez-Gutie´rrez and Morales-A´ vila (2016) described morphological characteristics for recognizing healthy krill as a frame of reference to infer pathological effects caused by symbiotic organisms. An individual krill with its metabolism in steady-state (in homeostasis) has a transparent body (an adaptation to decrease the risk of visual predators in the water column), red-brown chromatophores, a trans- lucent digestive gland (hepatopancreas), relatively large hepato-somatic index (proportion of the hepatopancreas length to that of the cephalothorax), fast and steady heartbeat, active peristaltic movements of the intestine, energetic and synchronous swimming movements, and regular growth, moulting and gonad development rates and functions. The pathognomonic (characteristics of specific parasites or diseases) in euphausiids are, so far, not well studied worldwide, compared with those in decapods of commercial value. However, the multiple symptoms of sickness or physiological response to epibionts, pathogens, or parasites in euphausiids include lack of transparency of the body (usually an opaque or Introduction 1

Fig. 1.1 Conceptual gradient of epibiont and parasite interactions with euphausiids classified according different trophic strategies (Lafferty and Kuris 2002). 3 Trematoda and Acanthocephala photographs taken by Jose´ Rau´l Morales-A´ vila and the rest of the photographs and micrographs taken by Jaime Go´mez- Gutie´rrez 4 1 Introduction pale whitish coloration, which indicates mechanical damage or failing homeostasis in the individual) (Hamner et. 1984), black spots on the exoskeleton (Miwa et al. 2008), and/or non-functional chromatophores. Additionally, gross signs of sickness include coloured (Go´mez-Gutie´rrez et al. 2003, 2006, 2012), mostly opaque, and sometimes pulsing digestive glands, a relative small hepato-somatic index and a contracted intestine that may lack peristaltic movement (signs of prolonged fasting). Also, slow or arrhythmic heartbeat, sluggish or erratic swimming (that sometimes can separate them from their conspecifics, lingering behind the krill schools or sometimes swimming solitary) (Hamner 1984; Hamner and Hamner 2000), irregular or slow growth (including shrinking), moulting, and gonad development (including re-absorption or castration). Infection by histophagous ciliates (parasitoids) is often indicated by swollen and beige-to-orange cephalothorax, dead euphausiids (Go´mez-Gutie´rrez et al. 2003, 2006, 2010, 2012, 2015a, b;Go´mez- Gutie´rrez and Morales-A´ vila 2016; Lynn et al. 2014). In recent years, ecologists have come to recognize the influence of parasites and diseases in regulating animal populations (Anderson and May 1978, 1981; Theódoride`s 1989;Go´mez-Gutie´rrez et al. 2003; Kuris et al. 2008). Parasites seem to be ubiquous in worldwide euphausiids distribution ranges, and presumably they co-evolve, taking biogeographic patterns similar to their hosts (Mauchline and Fisher 1969; Avdeev and Avdeeva 1989; Shimazu 2006;Go´mez-Gutie´rrez and Castellanos-Osorio 2010;Go´mez-Gutie´rrez and Morales-A´ vila 2016). Although several researchers have invested considerable research effort, they have been unsuccessful in detecting krill parasites in particular regions or periods (Kagei 1974, 1979; Kagei et al. 1978), or have found them only in low prevalences (Hurst 1984a, b; Morales-A´ vila et al. 2015; Morales-A´ vila 2016). Parasites have been detected, so far, in 49 of the 86-euphausiid species worldwide, but none are known as epibionts or parasites of any mesopelagic (Nematobrachion and Tessarabrachion) and bathypelagic (Bentheuphausia and Thysanopoda) species. The most studied krill species in terms of parasitic interactions are Euphausia pacifica, Euphausia similis, Euphausia superba, Meganyctiphanes norvegica, Nematoscelis difficilis, Nyctiphanes simplex, and Thysanoessa inermis (ordered alphabetically). Thus, diversity of epibionts and parasites (component community) has been well documented in relatively few euphausiid species (Komaki 1970; Shimazu 1975a, b, 2006;Go´mez-Gutie´rrez et al. 2010;Go´mez-Gutie´rrez and Morales-A´ vila 2016), and often for only a particular group of euphausiid parasites such as nematodes (Scott and Black 1960; Smith 1971, 1983a, b; Smith and Wootten 1978; Smith and Mooney 2005; Gregori et al. 2015a, b), cestodes (Shimazu 2006), trematodes (Shimazu 2006; Morales-A´ vila et al. 2015) and acanthocephalans (Gregori et al. 2012, 2013). Go´mez-Gutie´rrez et al. (2010) for Nyctiphanes simplex and Go´mez-Gutie´rrez and Morales-A´ vila (2016) for Euphausia superba are likely the first comprehensive reviews about parasites and diseases of a single euphausiid species. The numerically dominant subtropical krill N. simplex interacts with a diverse epibiont and parasitic species assemblage (Go´mez-Gutie´rrez et al. 2010). Go´mez-Gutie´rrez and Morales-A´ vila (2016) con- cluded that although the Antarctic krill, Euphausia superba, is among the best- 1 Introduction 5 studied species in the oceans; relatively few types of epibionts and parasites are currently known to interact with this key species. This results from a combination of apparently restricted invasion of symbionts into polar ecosystems and relative lack of parasite research effort carried out in the Southern Ocean on this key species. The reports of symbionts of E. superba (epibionts and parasites) date from no earlier than 1978 (Go´mez-Gutie´rrez and Morales-A´ vila 2016). However, there has been no recent comprehensive worldwide review about the types of euphausiid parasites, their life cycles, epizootiology, population and ecological impacts since the seminal reviews by Mauchline and Fisher (1969), Mauchline (1980), Shimazu (2006) and Spiridonov and Casanova (2010) (Fig. 1.2a, b). Go´mez-Gutie´rrez and Morales-A´ vila (2016) have added a summary for E. superba. Here, we update and summarize the current knowledge about euphausiid parasites on a worldwide basis, emphasizing life cycles, morphology, and distribution patterns (Fig. 1.2a, b). We estimate that 49 among the 86 currently valid species have at least one report of any type of epibiont or parasite (Fig. 1.2a). All nine krill species described between 1830 and 1860 decades and the only species described in the 1930 decade are known for having at least one type of parasite. Between 17% and 79% of the 68 krill species described between 1880 and 1910 decades have at least one record of epibiont or parasite. Between 1950 and 1980 decades only eight krill species were described. Two out of five (40%) krill species described in the 1960 decade are known for at least one type of parasite and the three species described in the 1950 and 1970–1980 decades are not known for any of their epibionts nor parasites (Fig. 1.2a). Overall, the krill species described in earlier decades are the best known for their epibiont or parasitic fauna. This may be explained because the relatively more recent described krill species are compara- tively less abundant and/or far less well studied in ecological and biological aspects than the oldest described krill species (Fig. 1.2a, b). G.O. Sars (1885) made the first known report of parasites infecting euphausiids from specimens collected during the landmark “Challenger Expedition,” detecting an ectoparasitic isopod (family Dajidae), and two helminth endoparasites (an acanthocephalan, and a trematode) (Fig. 1.2b). Mauchline and Fisher (1969) mentioned that parasites were known in 13 euphausiid species, only including two macroscopic parasites, a Dajidae isopod (Caullery 1897; Masi 1905) and the Ellobiopsids parasitizing euphausiids; those were then the best-studied krill parasites (Mauchline 1966). Mauchline and Fisher (1969) explicitly stated that no information was available on worms or protozoa that parasitize euphausiids. In a later monograph, Mauchline (1980) could have reported considerably more knowledge. He however reported only seven types of parasites including unnamed apostome ciliates attached to the euphausiid appendages (phoront stage); ellobiopsids (infesting 21 euphausiid species), Dajid isopods, Trematoda, Acanthocephala, Nematoda and Cestoda (see his Tables XXIV and XXV) (Fig. 1.2b). In their search of literature in university libraries (prior to internet technology) Mauchline and Fisher (1969) and Mauchline (1980) missed several of the then already known euphausiid-parasite records: the parasitoid dinoflagellates of the family Chytriodiniaceae that infect euphausiid eggs (Sars 1898; Dogiel 1906; Cachon and Cachon 1968), Apicomplexa Gregarinidae (Apstein 1911; Theódorides 6 1 Introduction

a 30 Cummulative number of

Total of species described 86 spp. 80 described krill species 25 No. of species with any parasite record

20 60

15 49 spp. 40

10 Total number of krill Total species described

20 5

0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 40 5 6 7 8 9 00 10 2 3 4 5 6 70 9 00 1 8 8 8 9 9 9 980 9 0 0 02 183 1 1 18 18 1 18 19 19 19 19 19 1 1 1 1 1 2 2 2 Decades b Cestoda Rhizocephala Nematoda Ciliata (parasitoids) Parasites in krill guts Molecular detection of Ciliata exuviotrophic Ciliata Opalinopsidae Ciliata hyperparasites Dinoflagellata parasitoid Apicomplexa Gregarinidae taxa that interact with krill Bacteria (chitinoclastic), fungus Ciliata Suctorida, Ellobiopsidae Bacillaripphyta diatoms epibionts Acanthocepahala, Trematoda, Dajidae Discovery of epibiont and parasitic 14 40

10 Lear (1963) Dogiel (1906) Lindley (1978) Apstein (1911) Hochberg (1982) G.O.Sars (1885) Polyanskii (1955) McClatchie (1990) Macdonald (1927) 8 Cleary et al. (2012) Landers et al. (2006) Shimazu et al. (1970) Kulka and Corey (1984)

6 Moore and Shirley (2000)

2 Number of parasite records 0 1880 1885 1890 1895 1900 1905 1910 1915 1920 1925 1930 1935 1940 1945 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 2015 2020 Years Mauchline and Fisher (1969) Bacillariophyta Ciliata (Suctorida) Ciliata (exuviotrophic) Ciliata (hyperparasite) Bacteria (Chitinoclastic) Rhizocephala, Cirrepedia Mauchline (1980) Fungus Bacteria Apicomplexa (Gregarinidae) Shimazu (2006) Isopoda (Dajidae) Ellobiopsidae Cestoda Trematoda Nematoda Acanthocephala Spiridonov and Casanova (2010) Dinoflagellata (parasitoid) Ciliata (parasitoid) Gómez-Gutiérrez and Morales-Ávila (2016)

Fig. 1.2 (a) Historical number of euphausiid species (Order Euphausiacea) described per decade (white bars) and same records, but including only species that currently are known at least one type of sumbiont (epibiont, parasite, parasitoid or micropredator) (black bars) and (b) Worldwide historical research on epibionts, parasites and parasitoids of euphausiids, showing when the pioneering work on each of the taxonomic groups that interact with euphausiids was published (colour arrows) and the major bibliographical reviews of euphausiid parasites (colour triangles) 1 Introduction 7 and Desportes 1975), ciliate Suctoridae (Macdonald 1927), chitin clastic bacteria in Nematoscelis sp. and fungus (Lear 1963), Chromidina ciliates (Hochberg 1971), exuviotrophic ciliates (Lindley 1978), and bacterial flora of E. superba (Kelly et al. 1978; Locati et al. 1979) (Fig. 1.2b). Mauchline and Fisher (1969) and Mauchline (1980) also missed several references published before 1980 of types of parasites mentioned in their Tables XXIV and XXV: Bonnier (1900) reviewing Dajidae family infesting euphausiids (then known as “Schizopodes”), Lo Bianco (1902) reporting the Dajidae Branchyophryxis sp. infesting Euphausia gibba, Drago and Albertelli (1975) for H. appendiculatus, Cornejo de Gonzańez and Antezana Jerez (1980) for T. fagei, Shimazu (1971, 1972) for trematods of E. similis, Shimazu et al. (1970), Kagei (1974, 1979), Slankis and Shevchenko (1974) for helminths and Oshima et al. (1968, 1969) about Anisakis sp. experimental infection of euphausiids (Fig. 1.2b). These omissions alone justify our integrative and relatively more comprehensive review. The historical records show when each new symbiotic taxonomic group that interacts with euphausiids was discovered (Fig. 1.2b). G.O. Sars (1898), in the first description of euphausiid embryos and larval stages, observed and drew Chytriodiniaceae from Meganyctiphanes norvegica eggs without recognizing them as parasitoids, but as odd “spermatospheres” showing ducts from the chorion of the egg to the embryo (Go´mez-Gutie´rrez et al. 2009). These parasitic dinoflagellates were observed again and then assigned as Gymnodinium to the dinoflagellates by Dogiel (1906) (they are currently known as dinoflagellates of the genus Chytriodinium)(Go´mez-Gutie´rrez et al. 2009). The 1960s to 2015 was a period with intensive research on parasites of euphausiids. The most recent discoveries were the first reports of hyperparasitism (ciliates that parasitize exuviotrophic apostome ciliates that infest euphausiid pleopods) (Landers et al. 2006) and of cryptic Pseudocollinia Apostome species (Go´mez- Gutie´rrez et al. 2006, 2012; Lynn et al. 2014) (Fig. 1.2b). Because of a now extensive and sometimes obscure recent literature, our review may miss several relevant references. Shimazu (2006) reviewed the taxonomy of trematodes and cestodes that infect euphausiids from the North Pacific, focusing mostly on his own lifetime of research (published in Japanese). His review mostly covers parasites of Euphausia similis, Euphausia diomedeae, Euphausia vallentini, Euphausia pacifica, Nematoscelis, Thysanoessa inermis, Thysanoessa raschi and Thysanoessa longipes from the North Pacific Ocean. As far as we know Cleary et al. (2012)is the first study detecting parasites in euphausiids (Meganyctiphanes norvegica) using only molecular methods (Fig. 1.2b). Recently, Go´mez-Gutie´rrez and Morales-A´ vila (2016) reviewed the parasites and diseases of the Antarctic krill Euphausia superba. Although this species is among the best studied in the Order Euphausiacea in biological and ecological aspects, reports of their parasites and diseases are relatively scarce (Go´mez-Gutie´r- rez and Morales-A´ vila 2016). So far, this species seems to interact with seven taxonomic groups of symbionts [epibionts: (1) exuviotrophic ciliates (Foettingeriidae) and (2) microplanktophagous ciliates (Suctoridae, Ephelota); pathogens, such as (3) chitinoclastic bacteria and (4) fungi; and trophically transmitted endoparasites, such as (5) Apicomplexa (Gregarinidae, Cephaloidophora), (6) nematodes infecting krill eggs (under laboratory conditions) and 8 1 Introduction

(7) histophagous parasites, such as Apostomatida ciliates of the family Pseudocollinidae] (Go´mez-Gutie´rrez and Morales-A´ vila 2016). Spiridonov and Casanova (2010) provided the most recent comprehensive review about the exter- nal and internal morphology, development and life cycle, physiology, geography, ecology and ethology, economic importance, phylogeny and systematics of the Order Euphausiacea. They included a relatively short review about symbionts and parasites, citing several of the most recent publications since Mauchline (1980). Spiridonov and Casanova (2010) mention ten out of sixteen known symbionts and parasites that interact with euphausiids worldwide: (1) apostome exuviotrophic ciliates (phoront stages) (Lindley 1978; Landers et al. 2006), (2) cysts of Chromidina spp. (Hochberg 1982), (3) Collinia ciliates (now known as Pseudocollinia) (Go´mez-Gutie´rrez et al. 2003), (4) Phtorophrya sp. (Landers et al. 2006), (5) gregarine Apicomplexa (Avdeev 1985), (6) Ellobiopsidae (Boschma 1948; Mauchline 1966; Cornejo de Gonzalez and Antezana Jerez 1980; Mooney and Shirley 2000), (7) Dajidae isopods, (8) Cestoda (Shimazu 1999), (9) Trematoda (Komaki 1970) and (10) Nematoda (Komaki 1970). Although there have been several attempts to identify euphausiid prey using exclusively genetic methods (PCR-DGGE) (Martin et al. 2006; Passmore et al. 2006;Tobe€ et al. 2010). Martin et al. (2006) briefly mentioned putative apicomplexan sequences of krill guts in their discussion section. Cleary et al. (2012) is, so far as we know, the first study that explicitly detected a euphausiid parasite using a DNA-based approach [peptide nucleic acid mediated polymerase chain reaction (PNA-PCR) clone-library sequencing of 18S rDNA] while studying in-situ feeding of a euphausiid. They discovered DNA sequences of unidentified gregarine parasites infecting the northern krill Meganyctiphanes norvegica. The northern krill can spend some time feeding near the sea floor with densities up to 104 individuals per cubic meter) (Youngbluth et al. 1989). Cleary et al. (2016) also discovered prey and parasites (a Digenea trematode, gregarines, Foettingeridae ciliates and Amoebophrya dinoflagellates) of Pseudocalanus copepods using the same genetic approach (accounting 17% of the total recovered sequences). However, gregarines can be free-living or gut-symbionts of animals; not all them are parasites. Environ- mental SSU rDNA surveys have significantly improved our understanding of micro eukaryotic diversity (Lima-Mendez et al. 2015). Several major taxa of micro eukaryotes, however, are still very poorly represented in these databases, and this is especially true for diverse groups of single-celled parasites, such as gregarine apicomplexans (Rueckert et al. 2011). Other relevant monographs have summarized complex life cycles of parasites infecting molluscs and crustaceans, but with no or scant references to epibionts or parasites of euphausiids (Bonnier 1900; Chatton and Lwoff 1935; Johnson 1983; Theódoride`s 1989; Bradbury 1994, 1996; Shields 1994; Morado and Small 1995; Nicol et al. 2000; Fernandez-Leborans and Tato-Porto 2000; Ohtsuka et al. 2000, 2011, 2015; Lynn 2008; Rohde 2005; Fernandez-Leborans 2009; Williams and Boyko et al. 2012; Skovgaard 2014; Baeza 2015; Ohtsuka et al. 2000, 2011, 2015). Four extensive reviews about parasites of zooplankton have updated and synthe- sized most of the knowledge published from 1980 to 2010 (Theódoride`s 1989; Ohtsuka et al. 2000, 2011, 2015). Those reviews included several mentions of the 1 Introduction 9 most recently discovered euphausiid parasites, particularly suctorian epibiont ciliates (Ephelota sp.), apicomplexa eugregarines (“sporozoans”), and helminth worms. Shields (1994), Coats (1999) and Go´mez et al. (2009) extensively reviewed parasitic dinoflagellates that invade, infest and infect marine crustaceans. Lima- Mendez et al. (2015) emphasized, using metagenomic, the role of alveolate parasitoids as top-down effectors of zooplankton and microphytoplankton population structure and functioning. However, the ecological impacts of such protist parasitoids in euphausiids were still unexplored, unquantified and, in general, little understood. They have only been studied in the northeast Pacific region (Go´mez- Gutie´rrez 2004;Go´mez-Gutie´rrez et al. 2003, 2006, 2009, 2010, 2012, 2015a, b; Lynn et al. 2014). Additionally, numerous studies have focused on parasites of functional host groups like molluscs, fish, sea birds, and marine mammals, for which euphausiids often play significant roles as intermediate or paratenic hosts (Smith 1984; Lambertsen 1986; Bradbury 1994; Marcogliese 1995; Muzaffar and Jones 2004; Baldwin et al. 2008). It is estimated that about 40% of all species are parasitic (Dobson et al. 2008). An average mammalian host species appears to harbour two species of cestodes, two trematodes, and four nematodes, and an acanthocephalan is found in every fourth mammalian species examinated (Dobson et al. 2008). Each bird species harbours on average three cestodes, two trematodes, three nematodes, and one acanthocephalan (Dobson et al. 2008). They claimed that none of these estimates take possible unrecognized cryptic species into account, but, in general, helminths that parasitize avian species seem to be less host-specific than those that parasitize mammals. Zooplankton, including euphausiids, typically are paratenic or intermediate hosts of multiple parasites with low specificity, facilitating their transmission to animals at higher tropic levels (Marcogliese 1995; Gregori et al. 2012, 2013, 2015a, b; Morales-A´ vila et al. 2015; Morales-A´ vila 2016) and creating a complex web of trophic interactions in the bentho-pelagic marine ecosystem (Frank et al. 2007; Lima-Mendez et al. 2015). However, euphausiids seem to be the final hosts (perhaps the only one) for several parasites, such as the exuviotrophic ciliates, Dajidae isopods, Gregarinidae, the ellobiopsid mesoparasite (parasitic organism that lives partly embedded in its host, usually with one end forming an anchor process) Thalassomyces fagei, and the histophagous ciliates Pseudocollinia, among others (Mauchline 1966; Shields and Go´mez-Gutie´rrez 1996; Landers et al. 2006; Go´mez-Gutie´rrez et al. 2003, 2006, 2012; Lynn et al. 2014). The most recent descriptions of parasite species infecting euphausiids are of Pseudocollinia (Capriulo and Small 1986;Go´mez-Gutie´rrez 2004;Go´mez-Gutie´r- rez et al. 2003, 2004, 2006, 2012; Lynn et al. 2014), opportunistic bacterial pathogens (Miwa et al. 2008;Go´mez-Gutie´rrez et al. 2015a), dinoflagellate endoparasitoids that infect euphausiid eggs (Go´mez-Gutie´rrez et al. 2009), nematodes and acanthocephalans (Gregori et al. 2012, 2013, 2015a, b), trematodes (Morales-A´ vila et al. 2015), and likely new species of apicomplexans parasitizing temperate and tropical euphausiids in the Pacific Ocean, including Nyctiphanes simplex and Nematoscelis difficilis in the Gulf of California (Go´mez-Gutie´rrez, unpublished data) (Fig. 1.2b). Other studies have focused on relatively better- known euphausiid parasites. They have advanced considerably not only the 10 1 Introduction taxonomy but also the ecological perspective, significantly increasing our understanding of life cycles and the impacts of parasites on euphausiid populations (Smith 1983a, b; Shimazu 2006; Takahashi et al. 2003, 2004, 2008, 2009, 2011; Takahashi 2012; Gregori et al. 2012, 2013, 2015a, b). Nevertheless, the taxonomy, life histories, physiology and epizootiology of the parasites of euphausiids are still poorly studied. Work remains to fill in ecological, physiological and evolutionary perspectives. This is partly related to the relatively low prevalences of most parasites (particularly the macroparasites), logistical difficulties to observe and detect them (without doubt more easily detected when krill are alive than when they are preserved), and the inherent complexities of each type of parasite that requires multiple hosts to complete its life cycle. Poor taxonomic knowledge and the relatively few experts on parasites of euphausiids are other difficulties. Here, we comprehensively summarize, when it is possible, taxonomic, ecological and integrative perspectives, telling what is currently known about the eons-long co-diversification process occurring worldwide among epibiont organisms, parasites, and parasitoids associated with euphausiids. This is largely possible because the taxonomy (Baker et al. 1990; Mauchline 1980, 1984; Brinton et al. 2000) and biogeographic patterns of the species of the Order Euphausiacea are well known (Brinton 1962, 1975; Mauchline and Fisher 1969; Brinton et al. 2000; Letessier et al. 2009, 2011). We want to emphasize the potential impact of epibionts and parasites on the vital rates, population dynamics of krill hosts and their food webs. Additionally, we propose several integrative hypotheses about the interactions among parasites and their hosts and the potential influence of parasites in the flux of carbon from the epipelagic ecosystem to deeper layers of the water column.

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