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Spatio-Temporal Dynamics of Parasites Infecting Diporeia Spp

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Spatio-Temporal Dynamics of Parasites Infecting Diporeia Spp Journal of Invertebrate Pathology 121 (2014) 37–45 Contents lists available at ScienceDirect Journal of Invertebrate Pathology journal homepage: www.elsevier.com/locate/jip Spatio-temporal dynamics of parasites infecting Diporeia spp. (Amphipoda, Gammaridae) in southern Lake Michigan (USA) ⇑ Andrew D. Winters a, Scott Fitzgerald b, Travis O. Brenden a, Thomas Nalepa c, Mohamed Faisal a,b, a Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824, USA b Pathobiology and Diagnostic Investigation, Michigan State University, East Lansing, MI 48824, USA c NOAA, Great Lakes Environmental Research Laboratory, 4840 S. State Road, Ann Arbor, MI 48108, USA article info abstract Article history: Since the 1990s, populations of the benthic amphipod Diporeia spp. (Diporeia) have sharply declined Received 3 December 2013 across much of the Laurentian Great Lakes. This study was undertaken to identify contemporary and his- Accepted 23 June 2014 torical community composition, structure, and dynamics of parasites infecting Diporeia collected from Available online 30 June 2014 nine sites in the southern basin of Lake Michigan, where declines of the amphipod have been well documented over the past 20 years. An additional aim of this study was to assess whether infection Keywords: dynamics and dreissenid densities could explain the declines in Diporeia densities that have occurred. Diporeia spp. We found that Diporeia were host to eight groups of uni- and multicellular pathogens. Of the 3082 amphi- Parasites pods analyzed, 1624 individuals (52.7%) were infected with at least one type of parasite. Ciliophora was Laurentian Great Lakes the most prevalent parasite (50.08% prevalence of infection), followed by Gregarinasina (2.79%), Microsporidia (0.68%), Cestoda (0.45%), Acanthocephala (0.36%), Haplosporidia (0.23%), Yeast (0.32%), and filamentous Fungi (0.10%). Considerable spatial and temporal variability were observed in parasite prevalences, with prevalences frequently appearing to cycle between low and high values. Parasite spe- cies belonging to Microsporidia and Haplosporidia were associated with tissue alteration and host inflammatory response; however, parasite prevalences explained very little in terms of Diporeia density declines at assessed sites. Despite these findings, we do not discount the possibility that parasitic infec- tions may have played a role in declining Diporeia densities in the Great Lakes, as the cyclical prevalences that were observed are possibly suggestive of parasitic outbreaks that are followed by die-offs at affected sites. This study suggests that if parasites have affected Diporeia densities in the Laurentian Great Lakes, then the relationship may be a complicated one. Ó 2014 Elsevier Inc. All rights reserved. 1. Introduction higher trophic levels and serve as coupling mechanisms between pelagic and benthic zones of the Great Lakes (Fitzgerald and Amphipods of the genus Diporeia (hereafter referred to as Gardner, 1993). Diporeia) occupy a central position in the foodweb of the Historically, Diporeia have been the most widespread and dom- Laurentian Great Lakes ecosystem (hereafter referred to as Great inant benthic macroinvertebrate in the Great Lakes, reaching den- Lakes). As an infaunal detritivore that feeds on pelagic material sities in excess of 14,000/m2 (Henson, 1966, 1970; Cook and that settles to the benthos, Diporeia are the foremost consumer Johnson, 1974). Over the last 20 years, Diporeia abundances have of primary production in the Great Lakes (Gardner et al., 1990). declined across much of the Great Lakes (Nalepa et al., 1998, Because Diporeia are important food resources for numerous Great 2007; Dermott and Kerec, 1997; Lozano et al., 2001; Barbiero Lakes fish species (Wells, 1980; Selgeby et al., 1994; Rand et al., et al., 2011). Due to the unique position of Diporeia in the foodweb 1995; Davis et al., 1997; Hondorp et al., 2005; Pothoven, 2005), and the fact that they once accounted for most of the benthic bio- they function as important conduits of nutrients and energy to mass in the lakes (Nalepa, 1989), it is believed that these large- scale declines have resulted in major foodweb restructuring in the Great Lakes (Nalepa et al., 1998). ⇑ Corresponding author. Permanent address: Department of Pathobiology and Several hypotheses have been proposed to explain Diporeia Diagnostic Investigation, College of Veterinary Medicine, Michigan State University, declines in the Great Lakes, including (1) greater predation East Lansing, MI 48824, USA. Fax: +1 517 432 2310. E-mail address: [email protected] (M. Faisal). stemming from increases in certain fish populations, such as lake http://dx.doi.org/10.1016/j.jip.2014.06.008 0022-2011/Ó 2014 Elsevier Inc. All rights reserved. 38 A.D. Winters et al. / Journal of Invertebrate Pathology 121 (2014) 37–45 whitefish Coregonus clupeaformis (Ebener et al., 2008), (2) Mayer’s hematoxylin and eosin (Luna, 1968). Additional diagnostic decreased dissolved oxygen concentration (Nalepa et al., 2005), features of parasites were determined by examination of selected (3) decreased food availability due to increased abundance of inva- sections stained with Giemsa (MHE, Luna, 1968), Grocott’s methe- sive, filter-feeding dreissenid mussels (Nalepa et al., 2006), (4) the namine silver (GMS, Luna, 1968), and Feulgen picro-methyl blue release of toxins by dreissenid mussels (Dermott et al., 2005), and (FPM, Farley, 1969) and Periodic acid Schiff (PAS, Lillie, 1965). (5) increased pollutants in sediments (Landrum et al., 2000). Sampling stations were chosen such that there was contrast in Although studies have been conducted exploring each of these location, depth, and the rate in which Diporeia densities declined hypotheses, the exact cause of the Diporeia declines remains over time (Fig. 1). Since, Diporeia declined more rapidly on the east unknown (Nalepa et al., 2009). In Lake Michigan, Diporeia side of the lake (A-1, H-22, H-21, EG-14) compared to the west side abundances were declining in the late 1990s despite what was (H-8, B-7, B-6, B-5) (Nalepa et al., 1998), samples were collected considered to be sufficient flux of organic matter reaching the ben- along an east-to-west gradient. Additionally, since populations thos (Nalepa et al., 2006) suggesting that declining abundances generally declined progressively from shallow to deep regions were not simply a result of competition with dreissenid mussels. (Nalepa et al., 2005), sites on the two sides of the lake were Similar questions have been raised as to whether predation, chem- matched by depth with depths ranging from 18 m to 108 m. The ical contamination, and low dissolved oxygen were of a sufficient 93-m site station (X-2) located on the far northeast side of the degree to be the sole cause of declining Diporeia abundances in southern basin was also chosen for analysis because Diporeia den- Lake Michigan (Nalepa et al., 2005). sity at this site was 10 per m2 in 2005, while densities at B-6 and Previous studies have demonstrated that Diporeia can host an EG-14 were >1000 per m2, and by 2010, populations were extir- array of aquatic pathogens (Messick et al., 2004; Messick, 2009; pated from X-2. We analyzed several amphipod samples collected Muzzall and Whelan, 2011), including a rickettsia-like bacterium, in 1992 and after, representing pre- and post-invasion of dreisse- Ciliophora, gregarines, helminthes, Haplosporidia, and Microspor- nids in the Great Lakes (Nalepa et al., 1998). Together these sam- idia. It has been suggested that parasitic infection, perhaps exacer- ples representing a span of 27 years were examined to provide bated by other stressor events such as pollution or climate change, an understanding of the diversity and prevalence of parasitic could have contributed to the population declines in Diporeia that infections and determine if there was any variation in diversity have occurred in the Great Lakes (Messick et al., 2004). The most or prevalence of parasitic infections associated with Diporeia comprehensive study to date of parasitic infection in Great Lakes populations from before or after the introduction of dreissenids. Diporeia was by Messick et al. (2004), who collected and assessed disease prevalence from Diporeia from multiple sites in lakes 2.2. Identification of organisms infecting Diporeia Huron and Michigan in 2000, and as far back as the mid- to late- 1980s for some southern Lake Michigan sites. Since the study of Taxonomic systems for groups of organisms infecting Diporeia Messick et al. (2004) was completed, there have been no additional were based on the following sources: Ciliophora (Lom and assays of parasitic infection in Diporeia. As well, we are not aware Dyková, 1992; Corliss, 1979), Haplosporidia (Sprague, 1979), of any attempts to relate declines in Diporeia abundance to para- Microsporidia (Wittner and Weiss, 1999), Yeast (de Becze, 1956), sitic infection or to assess the importance of parasitism relative filamentous Fungi (Dick, 1990), Gregarinasina (Levine, 1980), to other possible contributing factors, such as expansion of dreisse- Cestoda (Wardle and Mcleod, 1952; Yamaguti, 1959), and nid mussels. Such studies are important because they can help Acanthocephala (Amin, 2002). identify why Diporeia populations have declined or why the declines have been particularly severe in some lakes and particular areas (Barbiero et al., 2011). 2.3. Analysis of Diporeia parasite community assemblages The aim of this study was to conduct an in-depth analysis
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