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Parasite Infection Directly Impacts Escape Response and Stress Levels in Fish Bridie J © 2020. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2020) 223, jeb230904. doi:10.1242/jeb.230904 RESEARCH ARTICLE Parasite infection directly impacts escape response and stress levels in fish Bridie J. M. Allan1,2,3,*, Björn Illing2, Eric P. Fakan2,3, Pauline Narvaez2,3,4, Alexandra S. Grutter5, Paul C. Sikkel6,7, Eva C. McClure2,3,8, Jodie L. Rummer2 and Mark I. McCormick2,3 ABSTRACT behavioural and physiological phenotypes (for review, see McElroy Parasites can account for a substantial proportion of the biomass and de Buron, 2014). Unlike macropredators such as piscivores, in marine communities. As such, parasites play a significant micropredators (which we define broadly to include both parasites ecological role in ecosystem functioning via host interactions. Unlike and micropredators as defined more narrowly by Kuris and Lafferty, macropredators, such as large piscivores, micropredators, such as 2000, and Lafferty and Kuris, 2002) typically do not cause direct parasites, rarely cause direct mortality. Rather, micropredators impose mortality, but rather cause a constant drain on energetics, thus an energetic tax, thus significantly affecting host physiology and significantly affecting host physiology and behaviour (for review, behaviour via sublethal effects. Recent research suggests that see Barber, 2007). However, the magnitude of this change depends infection by gnathiid isopods (Crustacea) causes significant on the parasite type, parasitic loading and the size and ontogenetic physiological stress and increased mortality rates. However, it is stage of the host (Sun et al., 2012). For example, larval and juvenile unclear whether infection causes changes in the behaviours that fish are reported to be more vulnerable to the effects of infection underpin escape responses or changes in routine activity levels. than their adult counterparts, owing to low body reserves and high Moreover, it is poorly understood whether the cost of gnathiid infection metabolism (Strathmann et al., 2002; Grutter et al., 2011). manifests as an increase in cortisol. To investigate this, we examined Moreover, parasitic infection can also affect behaviours and the effect of experimental gnathiid infection on the swimming and physical attributes important for fleeing predators, such as escape performance of a newly settled coral reef fish and whether reducing visual acuity (Seppälä et al., 2005), limb malformation infection led to increased cortisol levels. We found that micropredation causing reductions in maximum jumping distance, burst swimming by a single gnathiid caused fast-start escape performance and speed and endurance (Goodman and Johnson, 2011), and reducing swimming behaviour to significantly decrease and cortisol levels to critical swimming speeds in adult and newly settled coral reef fishes double. Fast-start escape performance is an important predictor of (Binning et al., 2013; Grutter et al., 2011). recruit survival in the wild. As such, altered fitness-related traits and One of the most prevalent ectoparasites on coral reefs is gnathiid short-term stress, perhaps especially during early life stages, may isopods (Crustacea) (Grutter, 1994; Sikkel and Welicky, 2019). result in large scale changes in the number of fish that successfully Gnathiids, mobile temporary parasites of fish, feed using a trophic recruit to adult populations. strategy that might best be referred to as micropredation (Kuris and Lafferty, 2000; Lafferty and Kuris, 2002). Micropredators attack KEY WORDS: Escape performance, Fish behaviour, Micropredator, multiple prey (hosts), much like predators do, but an individual Predator–prey interactions micropredator’s effect on its prey tends to be small. Micropredators of vertebrate hosts, such as ticks, mosquitos and gnathiids, briefly feed INTRODUCTION on blood and are not transmitted trophically. Because micropredators Parasites can reach high biomass in marine communities (Kuris feed on several prey individuals, they also do not benefit from et al., 2008) and make up around 40% of the total biodiversity on minimising damage to prey (Barber et al., 2000) and can rapidly Earth, making them one of the most successful modes of life (Poulin abandon their prey if it is incapacitated (Murray, 1990; Lehmann, and Morand, 2000; Hatcher and Dunn, 2011). As such, parasites 1993). These reef-based parasites feed on a variety of coral reef fish play a significant role in ecosystem functioning as they exert sub- hosts from teleosts to elasmobranchs and on all host ontogenetic lethal effects on their host where they can modify and manipulate stages (Grutter and Poulin, 1998; Grutter et al., 2017). As such, they can cause significant physiological stress such as increased oxygen consumption (Grutter et al., 2011), reduced haematocrit (Jones and 1Department of Marine Science, University of Otāgo, Dunedin 9054, New Zealand. Grutter, 2005), increased cortisol load (Triki et al., 2016) and even 2ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, QLD 4811, Australia. 3Department of Marine Biology and Aquaculture, mortality (Hayes et al., 2011). Previous work by Grutter et al. (2011) James Cook University, Townsville, QLD 4811, Australia. 4Centre for Sustainable estimated that a single gnathiid can consume up to 85% of the blood Tropical Fisheries and Aquaculture, James Cook University, Townsville, QLD 4811, volume of a late-stage larval damselfish, which has the potential to Australia. 5School of Biological Sciences, The University of Queensland, St Lucia, QLD 4072, Australia. 6Department of Biological Sciences, Arkansas State significantly affect behaviours that rely on aerobic activities, such as University, Jonesboro, AR 72467, USA. 7Water Research Group, Unit for swimming (Gallaugher et al., 1995; Grutter et al., 2011). Reduced Environmental Sciences and Management, North-West University, Potchefstroom swimming performance can affect the way in which a fish interacts 2520, South Africa. 8Australian Rivers Institute, Griffith University, Gold Coast, QLD 4215, Australia. with conspecifics and predators and whether it can settle successfully to the benthic environment (Allan et al., 2013; Grutter et al., 2011). *Author for correspondence ([email protected]) When coral reef fishes recruit to the benthic environment, it is B.J.M.A., 0000-0002-5991-9711; B.I., 0000-0002-5217-805X reported that predator-induced mortality can be absolute, but averages 60% within the first few days of settlement (Almany and Received 12 June 2020; Accepted 26 June 2020 Webster, 2006). Predator avoidance and evasion are key ecological Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2020) 223, jeb230904. doi:10.1242/jeb.230904 traits that are directly related to growth and survival. When a predator ambon damselfish, Pomacentrus amboinensis Bleeker 1868 attacks, prey are faced with a series of decisions, such as how fast to (Pomacentridae) [standard length range 9–12 mm, mean±s.d. 10.3 respond, which direction to turn, and how fast and how far to escape ±0.05 mm] were collected using light traps (Meekan et al., 2001) in in an overall whole-organism behaviour called a fast start (for review, the waters off Lizard Island (14°40′S, 145°28′E) in the northern see Domenici and Blake, 1997). Fast-start escape behaviour can Great Barrier Reef, Australia. This species is a common component significantly increase the probability of prey escape (Walker et al., of the benthic fish fauna of Indo-Pacific reefs, and adults inhabit 2005; Allan et al., 2013, 2015, 2017). The effectiveness of fast-start sandy areas of lagoons and inshore reefs. Pomacentrus amboinensis escape behaviour is a consequence of body morphology, muscle naturally settle on patch reef environments near the continuous reef. mass and muscle cell physiology and energy reserves (Langerhans, In this habitat, juveniles are exposed to reef-associated gnathiids 2009). Fast starts are characterised by rapid acceleration, which is and macropredators that use a variety of feeding modes from driven by the rapid anaerobically powered contraction of large ambush (lizardfish Synodus dermatogenys and the small grouper myotomal blocks of fast glycolytic muscle (Rome et al., 1988; Cephalopholis microprion) to pursuit (dottybacks Pseudochromis Josephson, 1993). Although anaerobically powered, fast starts are a fuscus and wrasse Thalassoma lunare). These fishes can be strenuous form of activity in which the active muscles require more observed to prey on juveniles that venture too far from shelter oxygen than can be supplied during the period of activity. Therefore, (McCormick, 2012), including the species used in this study, an oxygen debt is accrued that needs to be repaid via aerobic P. amboinensis. After capture, P. amboinensis were transferred from metabolism (Scarabello et al., 1991). light traps to aquaria (65×35×30 cm) with aeration and water flow To date, few studies have addressed the effects of parasitic load for a minimum of 48 h before use in trials. Coral reef fish recruits, on fast-start escape behaviours. Blake et al. (2006) examined the when captured using light traps, habituate to life in aquaria effects of parasite load on the C-start performance of the three- extremely quickly and will feed within several hours following spined stickleback, Gasterosteus aculeatus, and found negative removal from light traps. effects on escape kinematics (Blake et al., 2006). By contrast, Binning et al. (2014)
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