Copepod and monogenean infection of fish under sea surface temperature anomalies
Introduction
Parasitic copepods (Crustacea: Copepoda) and monogeneans (Platyhelminthes: Monogenea) are two of the most common ectoparasites on marine fish. Both have a direct lifecycle in which early developmental stages (larvae) are free-living and juveniles and adults are parasitic. The development of parasitic copepods involves a number of stages, which may vary among families. In Caligidae, which is the most common family of parasitic copepods on marine fish, mature females produce eggs that hatch as free-swimming nauplii. There are two naupliar stages followed by the copepodid (the infective stage that locates a host), four chalimus and/or pre-adult stages, and then the adult (Venmathi-Maran et al., 2013). Most monogeneans lay eggs that hatch into larvae known as oncomiracidia, which must attach to a specific host species. A few species are viviparous, giving birth to young parasites, which attach to the same host as the parent and may subsequently transfer to a new host when hosts touch (Jansen and Bakke, 1991; Olstad et al., 2006; Brazenor et al., 2020; Hoai, 2020).
During their development, parasitic copepods and monogeneans are directly exposed to variability in water conditions. Water temperature has a particularly strong influence on their lifecycle. The development time, adult body size, and reproductive outputs of caligid copepods are negatively associated with increasing temperature (Samsing et al., 2016; Hamre et al., 2019). Similarly, evidence from Neobenedenia girellae suggests that at low temperatures, monogeneans exhibit slower production of larger, energy-dense eggs, whereas at high temperatures, monogeneans mature faster and produce less energy-rich eggs at a faster rate (Brazenor et al., 2020). Infection levels of parasites may, therefore, peak during warm periods. However, available evidence indicates that seasonal dynamics of fish parasitic infection are far from universal. Strong seasonal dynamics have been found for some parasites and host taxa in certain habitats, but not for others (Poulin, 2020). Additionally, it has been argued that pulse heat events, which are expected to be more frequent and intense in the future, may increase or reduce the transmission of parasites. As no universal patterns have been detected, researchers must measure the effects of warming on focal hosts, parasites, and corresponding communities to develop predictions for a particular system (Claar and Wood, 2020).
The Gulf of California (GC) is a biodiversity hotspot and the most important fishing region in Mexico (Lluch-Cota et al., 2007). This enclosed area is subject to overfishing, loss of biodiversity and habitats, pollution, climate variability, and climate change (Páez-Osuna et al., 2016). The ecological variability in the GC is affected by El Niño-Southern Oscillation (ENSO) events (Lluch-Cota et al., 2010; Herrera-Cervantes et al., 2020) because of its connection to the Pacific Ocean. However, there is a limited knowledge of the effects of ENSO on the dynamics of marine parasites.
In the present study, we analyzed changes in the prevalence and intensity of infection of Pacific sierra (Scomberomorus sierra) from the southeastern GC by parasitic copepods and monogeneans, during a six-year period (2015 to 2021). This period included anomalous warm and cold episodes influenced, respectively, by the very strong El Niño event in 2015–2016 and the moderate La Niña in 2020–2021 (Fig. 1). Scomberomorus sierra is distributed in the eastern tropical and subtropical Pacific and is particularly abundant in the southeastern GC, representing an economically important resource (see Torres-Rojas et al., 2020, and references therein). In Sinaloa state, during 2015 and 2016, around 2000 tons live weight was landed, while for the period 2017–2019 the values were greater than 3000 tons (SIPESCA, 2019). The commercial size captured in the study area ranges from 10 to 75 cm in fork length (FL) and the fishing effort is supported by organisms of 35 to 44 cm FL (Aguirre-Villaseñor et al., 2006). In addition to its abundance, we selected S. sierra because it is a host species for a range of metazoan parasites, including copepods and monogeneans, as recently reported by Santos-Bustos et al. (2020).
Section snippets
Study area and environmental variables
The southeastern GC is influenced by coastal ecosystems, the North Equatorial Current, and the California Current. It is a highly productive ecosystem, and its structure and function are influenced by climatic variability, with lower resilience during periods of high temperature variation (Hernández-Padilla et al., 2021). In the present study, a location in the southeastern GC (23.05° N, 106.38° W) was selected to analyze temporal variations in sea surface temperature (SST) and sea surface
Results
The average FL (± SD) of the fish varied between 40.2 ± 2.4 cm in January 2015 and 55.5 ± 8.1 cm in June 2015. There were significant differences (F = 6.252, P < 0.001), with fish in six months (January, and February 2015; April 2017; November, and December 2020; and January 2021) being smaller than fish in the other months (P < 0.05) (Fig. 2A). Likewise, fish caught during normal episodes were significantly larger than those caught during either warm or cold episodes (F = 9.662, P < 0.001) (
Copepods
In the present study there was no strong evidence that anomalous warming in the ocean induces increases in infection of fish by parasitic copepods. One would expect that high temperatures have a positive effect on the prevalence and intensity of these parasites. In previous experiments, the copepods Caligus rogercresseyi and Lepeophtheirus salmonis, which are found in temperate regions, showed faster development, higher egg production, and increased infection success at higher than at lower
Conclusion
The results of our study indicate that while the typical intensity of parasitic copepods and monogeneans does not change between warm or cold conditions, their prevalence may increase when water temperatures rise, but only within their thermal limits. Warm anomalies of more than 2 °C above average appear to negatively affect parasite population size. Taken together, these findings support the observations of Brazenor et al. (2020), who concluded that ectoparasites have evolved substantial
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
Rosa M. Medina Guerrero (CIAD-Mazatlán) helped with fish examination. Nancy Bárcenas de los Santos and Luis García Prieto (IB-UNAM) assisted with the identification of monogenean species. EME is grateful to CONACyT for support through program “Cátedras” (Project No. 2137). HAV thanks to the “Proyecto Escama”, CRIAP-Mazatlán. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
References (40)
- et al.
Temperature alters reproduction and maternal provisioning in a fish ectoparasite
Int. J. Parasitol.
(2020) - et al.
Pulse heat stress and parasitism in a warming world
Trends Ecol. Evol.
(2020) - et al.
Structure and function of the southeastern Gulf of California ecosystem during low and high sea surface temperature variability
Reg. Stud. Mar. Sci.
(2021) - et al.
Interannual variability of surfaces satellite-derived chlorophyll concentration in the bay of La Paz, Mexico, during 2003−2018 period: the ENSO signature
Cont. Shelf Res.
(2020) - et al.
The influence of different water temperatures on Neobenedenia girellae (Monogenea) infection, parasite growth, egg production and emerging second generation on amberjack Seriola dumerili (Carangidae) and the histopathological effect of this parasite on fish skin
Aquaculture.
(2010) - et al.
Life in the fast lane: temperature, density and host species impact survival and growth of the fish ectoparasite Argulus foliaceus
J. Therm. Biol.
(2020) - et al.
The Gulf of California: review of ecosystem status and sustainability challenges
Prog. Oceanogr.
(2007) - et al.
Changing climate in the Gulf of California
Prog. Oceanogr.
(2010) - et al.
Early development of the ectoparasite Caligus rogercresseyi under combined salinity and temperature gradients
Aquaculture
(2018) - et al.
Early development and metabolic rate of the sea louse Caligus rogercresseyi under different scenarios of temperature and pCO2
Mar. Environ. Res.
(2020)
Environmental status of the Gulf of California: a review of responses to climate change and climate variability
Earth-Sci. Rev.
Meta-analysis of seasonal dynamics of parasite infections in aquatic ecosystems
Int. J. Parasitol.
Biostatistics for parasitologists - a primer to quantitative parasitology
Trends Parasitol.
Effects of temperature on fecundity in vitro, egg hatching and reproductive development of Benedenia seriolae and Zeuxapta seriolae (Monogenea) parasitic on yellowtail kingfish Seriola lalandi
Int. J. Parasitol.
Biological indicators for the Pacific sierra (Scomberomorus sierra) fishery in the southern Gulf of California, Mexico
Cienc. Mar.
Ectoparasites and endoparasites of fish form networks with different structures
Parasitology.
Effects of temperature and salinity on the life cycle of Neobenedenia sp. (Monogenea: Capsalidae) infecting farmed barramundi (Lates calcarifer)
Parasitol. Res.
Visualization of regression models using visreg
R J.
The origins of the anomalous warming in the California coastal ocean and San Francisco Bay during 2014-2016
J. Geophys. Res.-Oceans.
The effect of temperature on ability of Lepeophtheirus salmonis to infect and persist on Atlantic salmon
J. Fish Dis.
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