Blood Parasite Biodiversity of Reef-Associated Fishes of the Eastern Caribbean

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Blood Parasite Biodiversity of Reef-Associated Fishes of the Eastern Caribbean Vol. 533: 1–13, 2015 MARINE ECOLOGY PROGRESS SERIES Published August 6 doi: 10.3354/meps11430 Mar Ecol Prog Ser FREE CCESS FEATURE ARTICLE A Blood parasite biodiversity of reef-associated fishes of the eastern Caribbean Courtney A. Cook1, Paul C. Sikkel1,2, Lance P. Renoux2, Nico J. Smit1,* 1Water Research Group, Unit for Environmental Sciences and Management, North-West University, Potchefstroom 2520, South Africa 2Department of Biological Sciences and Environmental Sciences Program, Arkansas State University, State University, Arkansas 72467, USA ABSTRACT: Parasitic micro-organisms can influence multiple ecological processes, from growth, mortality, and behavior, to community structure and trophic interactions, yet are typically ignored components of marine biodiversity. We collected 1298 blood samples from reef fishes off 6 eastern Caribbean islands, repre- senting 27 families, 57 genera and 103 species, in - cluding invasive Indo-Pacific lionfish. Members of 14 species from 8 families were infected, comprising damselfishes (Pomacentridae), parrotfishes (Scaridae), mullet (Mugilidae), jacks (Caranjidae), Blennies (Blen- neidae and Labrisomidae), snappers (Lutjanidae), and angelfishes (Pomacanthidae). None of the 8 distinct blood parasites found fit descriptions of other Ca - ribbean parasites, but resembled typical Haemogre - garina-like intraerythrocytic parasites and Haemo- hormidium-like parasites collected from fishes on the Great Barrier Reef (GBR), Australia. No blood parasites were found in lionfish and there was surprisingly little overlap in the families of Caribbean and GBR fishes. Most infected species were strongly diurnal. The high Survey of eastern Caribbean reef-associated fishes shows a incidence of infection in Stegastes damselfishes was high biodiversity of unique blood parasites particularly surprising and has potentially important Image: Courtney A. Cook, Edward C. Netherlands ecological consequences, given that damselfishes in- fluence benthic community structure and are prey for reef piscivores. Gnathiid isopods, an apparent vector KEY WORDS: Coral reefs · Marine reserves · Recovery of apicomplexan blood parasites in other systems, rates · Spatial comparisons · Temporal monitoring · were common at sampling sites and collected for Philippines use in transmission experiments. Haemogregarina- Resale or republication not permitted without like parasites were taken up by gnathiids that fed written consent of the publisher on infected blennies. By comparison, when gnathiids fed on Stegastes damselfish infected with a Haemo - hormidium-like parasite, no parasites were found. INTRODUCTION This study reveals the high biodiversity of haemopara- sites infecting eastern Caribbean reef fishes, and The major challenge facing ecologists, conserva- highlights the need for additional research throughout tionists, and managers of marine reef ecosystems the Caribbean and in other tropical reef systems. is to understand the complex biological interactions *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 2 Mar Ecol Prog Ser 533: 1–13, 2015 that occur within and between reef-associated ha - Laird (1951) described Haemogregarina salariasi bitats and how these interactions are affected by from his survey of 193 fishes of 22 species from the anthropogenic activity. Research on the biological reefs off Fiji, however this species was later syn- diversity and complexity of marine ecosystems has onomised with H. bigemina (see Siddall 1995). Saun- historically focused on macrofauna that are easily ders (1954, 1955, 1958b, 1964) reported, from her seen and surveyed by scientists. Thus, the under- combined sample of 2640 fishes from 57 species and standing of the diversity and function of micro - 23 families from the Caribbean region, one unnamed organsims constitutes a current frontier in research haemogregarine, along with Haemogregarina achiri, on marine biocomplexity (e.g. Das et al. 2006). Many H. dasyatis and H. brevoortiae (Saunders 1964). Saun- of these organisms function as parasites. Indeed, ders (1960) also described H. rubrimarensis from the parasitism is the most common animal lifestyle and Red Sea samples of 1541 fishes from 104 species. thus the most common biological interaction (Hud- Along with these descriptions, Saunders (1954, 1955, son et al. 2006). Because of their effects on host 1958a,b, 1959a, 1960, 1964, 1966) reported H. bigem- population dynamics, parasites directly or indirectly ina from all collection localities—a haemogregarine influence biodiversity of ecological communities now thought to be of questionable cosmo politan dis- in general (e.g. Wood et al. 2007, Hatcher & Dunn tribution (see Davies et al. 2004). Similarly, from the 2011). GBR, Burreson (1989) reported 3 species of Hae - While recent studies of marine parasites have mogregarina in a survey including 69 fishes belong- made substantial contributions to our understanding ing to 28 species from Heron Island, and Smit et al. of the role of parasites in ecosystems generally (Hux- (2006) documented 4 haemogregarines during a sur- ham et al. 1995, Thomas et al. 1998, Mouritsen & vey involving 497 fishes from 78 species from Lizard Poulin 2005, Thompson et al. 2005, Arias-González & Island. In both surveys of the GBR above, non- Morand 2006, Lafferty et al. 2006, Kuris et al. 2008, haemogregarine blood parasites were reported along Dunne et al. 2013), our understanding of the diversity with observations of H. bigemina or H. bigemina-like and role of parasites in marine systems has been haemogregarines. These included 2 species of Try- driven primarily by studies of easily accessible, ‘model’ panosoma and 1 species of Haemohormidium from systems, commercially important species, and oppor- fishes off Heron Island (Burreson 1989), as well tunistic observations (reviewed by Poulin et al. 2014). as a Haemohormidium-like infection from fishes off Given that the discovery of marine parasite species Lizard Island (Smit et al. 2006). Astonishingly, with over time continues to accelerate (rather than asymp- all the surveys carried out by Saunders (1954, 1955, tote), simply characterizing the parasite fauna in ma - 1958a,b, 1959a,b, 1966), non-haemogregarine blood rine systems constitutes a major challenge to under- parasites such as those above collected from other standing their role in marine communities (Poulin et coral reef environments were not identified, discov- al. 2014). ered, or described from reef-associated fishes of the Because of their ease of access, working conditions Caribbean, except for a single record where Saun- that facilitate extended time in the field, and their ders (1959b) described a trypanosome, Trypanosoma high biodiversity, coral reefs are one of the most balistes Saunders, 1959, from Balistes capriscus (Bal- intensively studied marine ecosystems. However, istidae). This is particularly interesting since Saun- parasites may comprise as much as 80% of the ders (1960) did describe other non-haemogregarine organisms on tropical reefs (Rohde 2002), and few infections from fishes of the Red Sea including a coral reef ecologists are trained in parasitology. Ini- species of Babesiosoma and Dactylosoma. While tial efforts to characterize blood parasites in coral Saunders’ efforts were impressive, her studies fo- reef fishes were conducted in the 1950s and 1960s by cused on species commonly caught in local fisheries, Laird (1951) working in Fiji, and by Saunders (1954, including some pelagic species. In addition, her stud- 1955, 1958a,b, 1959a,b, 1960, 1964, 1966) working ies, as with those of Laird (1951), were conducted in the Caribbean and Red Sea. Based on the wide- using inferior (by modern standards) micro scopy, and spread occurrence of haemogregarine apicomplex- included neither photographic evidence nor voucher ans in terrestrial vertebrates, these studies focused specimens. on haemogregarines. Subsequent studies were not While little is known about blood parasites of coral conducted until over 20 yr later (Burreson 1989), and reef fishes, even less is known about how they are then again not until after the turn of the century (Smit transmitted (Smit et al. 2006), with few attempts at et al. 2006, Curtis et al. 2013), all focused on the vector identification and experimental transmission Great Barrier Reef (GBR). (Smit et al. 2006, Curtis et al. 2013). Furthermore, Cook et al.: Caribbean fish blood parasites 3 since haemogregarines are the most commonly re - Caribbean region (Saunders 1955, 1958a,b, 1959a,b, corded blood parasites of coral reef fishes, the focus 1964, 1966). Fish were collected over a period of of transmission studies has been on these parasites. 11 mo (June 2012 up to and including April 2013) by Leeches were for a long period assumed to be the divers using hand nets and modified cast nets main vectors of these fish blood parasites, particu- as described in Sikkel et al. (2009a), or obtained larly of haemogregarines (Davies & Smit 2001, Smit from local fishermen. Collection sites included (from et al. 2006). However, Davies & Johnston (1976) and east to west) St. Maarten (18.06° N, 63.05° W), Saba Davies (1982, 1995) proposed that gnathiid larvae (17.63° N, 63.23° W), Guana Island, British Virgin (Isopoda: Gnathiidae) may be vectors of the cosmo- Islands (18.50° N, 64.63° W), St. John, US Virgin politan H. bigemina. This suggestion was later sup- Islands (18.33° N, 64.73° W), St. Thomas, US Virgin ported by observations made by Davies et al. (1994), Is lands (18.33°
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