Parasite infection directly impacts escape response and stress levels in fish

Abstract

Parasites can account for a substantial proportion of the biomass in marine communities. As such, parasites play a significant ecological role in ecosystem functioning via host interactions. Unlike macropredators, such as large piscivores, micropredators, such as parasites, rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significantly affecting host physiology and behaviour via sublethal effects. Recent research suggests that infection by gnathiid isopods (Crustacea) causes significant physiological stress and increased mortality rates. However, it is unclear whether infection causes changes in the behaviours that underpin escape responses or changes in routine activity levels. Moreover, it is poorly understood whether the cost of gnathiid infection manifests as an increase in cortisol. To investigate this, we examined the effect of experimental gnathiid infection on the swimming and escape performance of a newly settled coral reef fish and whether infection led to increased cortisol levels. We found that micropredation by a single gnathiid caused fast-start escape performance and swimming behaviour to significantly decrease and cortisol levels to double. Fast-start escape performance is an important predictor of recruit survival in the wild. As such, altered fitness-related traits and short-term stress, perhaps especially during early life stages, may result in large scale changes in the number of fish that successfully recruit to adult populations.

Habitat associations and impacts on a juvenile fish host by a temperate gnathiid isopod

“…Although recent studies have reported decreased sustained swimming in parasitized fish ( Grutter et al, 2011 ; Allan et al, 2020 ), we found that infested individuals performed equally well as uninfested conspecifics in almost all burst and ambient swimming metrics. Our findings are consistent with a similar study by Östlund-Nilsson et al (2005) , which examined the impact of Anilocra sp., a much larger temporary ectoparasite, on fish swimming performance in the cardinal fish Cheliodipterus quinquelineatus .…”

“…The ability to escape a predator and forage efficiently are key behaviors influencing the survival of fishes. Swimming speed and behavior are often used as measures of the performance capabilities of fish, as they are important for predator avoidance, foraging, or finding suitable habitat ( Green and Fisher, 2004 ; Herbert and Steffensen 2005 ; Binning et al, 2014 ; Allan et al, 2020 ). Escape responses involve fast-start swimming, classified as a high-energy swimming burst, either from rest or from a steady-state swim, and are critical in the ability of mobile fish prey to escape their predators ( Batty and Blaxter, 1992 ; Domenici and Blake, 1997 ; Walker et al, 2005 ).…”

“…The susceptibility of individual fish to the same level of gnathiid infestation is not uniform among species; susceptibility may be driven by the scale thickness of a fish, scale type, cortisol response, or even mucus secretions that act as a protective cocoon ( Nagel and Grutter, 2007 ; Sikkel et al, 2011 , 2014 ; Coile and Sikkel, 2013 ). Most recently, Allan et al (2020) , found that a single gnathiid caused fast-start performance and swimming behavior to significantly decrease in recently settled Pomacentrus amboinensis . Similarly, Sellers et al (2019) found that sub-lethal gnathiid loads negatively impacted the ability of juvenile Stegastes leucostictus to defend a territory against an uninfected conspecific of similar size.…”

“…We assessed how fish size category (small and large) and gnathiid treatment level (control, low, medium, high) impacted a series of fish swimming response variables associated with ambient and burst swimming. Response variables, including cumulative distance traveled (mm), mean velocity while traveling (mm/s), response latency (ms), duration of the burst response (ms), mean burst velocity (mm/s), maximum velocity reached during the burst response (mm/s), and cumulative distance traveled during the burst response (mm) were tested using multivariate analysis of variance (MANOVA, Allan et al, 2020 ; Friedrich et al, 2018 ) with fish size category (small and large) and gnathiid treatment level (control, low, medium, high) as fixed factors, and the interaction between treatment and size class. Residual plots were examined to inform MANOVA assumptions of multivariate homogeneity and normality.…”

“…In cases of extreme infestation, they can cause death in adult hosts ( Mugridge and Stallybras, 1983 ; Hayes et al, 2011 ). However, for juvenile fishes, even a single gnathiid can prove fatal ( Grutter et al, 2008 , 2017 ; Artim et al, 2015 ; Sellers et al, 2019 ), and sub-lethal infestation can impact performance ( Sellers et al, 2019 ; Allan et al, 2020 ).…”