Early development and metabolic rate of the sea louse Caligus rogercresseyi under different scenarios of temperature and pCO₂

Highlights

• The temperature has a significant effect on the hatching time of C. royercresseyi.

• Combination of pCO₂ and temperature has a significant effect on survival in C. rogercresseyi.

• The combination of pCO₂ and temperature had no impact on the size of nauplius I, nauplius II and copepodid stage.

• Only the temperature has a significant effect on oxygen consumption rate of C. royercresseyi.

Abstract

Anthropogenic CO₂ emissions have led to ocean acidification and a rise in the temperature. The present study evaluates the effects of temperature (10, 15 and 20 °C) and pCO₂ (400 and 1200 μatm) on the early development and oxygen consumption rate (OCR) of the sea louse Caligus rogercresseyi. Only temperature has an effect on the hatching and development times of nauplius I. But both factors affected the development time of nauplius II (<temperature = longer development time). Copepodid survival time was also affected by temperature and pCO₂, at 10 °C and 400 μatm, survival was 30 and 44% longer than at 15 and 20 °C. OCRs were impacted by temperature but not by pCO₂. In all treatments, OCR was lower for nauplius II than for the copepodid. Our results show the need to further evaluate the effects of a combination of environmental drivers on the performance of C. rogercresseyi, in a changing and uncertain future.

Introduction

Climate change, driven by the rapid release of anthropogenic CO₂ into the atmosphere is causing an increase in seawater temperature, “ocean warming”, and at the same time a decrease in seawater pH, “ocean acidification” (IPCC, 2013; Duarte et al., 2014; Lee et al., 2017). Since preindustrial times ocean acidity has increased 26% and unabated CO₂ emissions are predicted to cause the acidity to increase by 170% during this century (IPCC, 2013). Several economic activities, such as aquaculture, occur in the marine realm and will experience the combined effects of elevated temperature and CO_2, which may influence the intensity and frequency of pathogen outbreaks (Ellis et al., 2017).

Elevated pCO₂ can cause alterations in the physiological performance of organisms (Navarro et al., 2013; Almén et al., 2017; Mangan et al., 2017). Additionally, severe behavioral changes, such as in the ability to avoid predators, obtain food, mating and swimming capacity, have been recorded in both mollusks and crustaceans as consequence of high levels of pCO₂ (Briffa et al., 2012; Navarro et al., 2013; Almén et al., 2017; Wang et al., 2018; Porteus et al., 2018). In copepods, high levels of pCO₂ can negatively affect survival rate, respiration rate, hatching success and development (Wang et al., 2018). For example, survival rates of Oithona similis nauplii and adults were significantly decreased by 20 and 40% at 700 and 1000 μatm, respectively, compared to the control treatment (370 μatm) (Lewis et al., 2013). Similar effects have also been observed in Acartia tonsa (Cripps et al., 2014), where elevated pCO₂ (1000 μatm) affected adult and nauplii survival rates. Based on previous studies, it has been suggested that the earlier developmental stages of copepods, especially the nauplii stage, are the most sensitive to ocean acidification (Wang et al., 2018). On the other hand, the effect of temperature on the physiological performance of several marine invertebrate species has been widely documented (Clarke, 1987; Thatje and Hall, 2016; Colpo and Lopez-Greco, 2017). In ectotherms, higher temperatures lead to an increased metabolism (e.g. higher respiration rate) (Thompson et al., 2019). In copepods, temperature directly affects the respiration and growth rates, accelerating them at increased temperatures and decreasing/delaying them with decreasing temperatures (Escribano et al., 1997; Montory et al., 2018; Heine et al., 2019; Hamre et al., 2019; Scheffler et al., 2019). Elevated temperatures shortened the developmental time and life cycle of the salmonid ectoparasite, Lepeophtheirus salmonis in the northern hemisphere (Groner et al., 2016; Hamre et al., 2019). For this ectoparasite, temperature has a particularly marked effect on the duration of the non-infective stages (nauplius I and II), varying from 50.0 h at 15 °C to 223.3 h at 5 °C, (Tully, 1992). Similar results with different temperature treatments have also been recorded for the copepod ectoparasite Caligus rogercresseyi (González and Carvajal, 2003; Montory et al., 2018), a response that could drastically affect the epidemiology of this ectoparasite.

Growing evidence shows that environmental drivers act synergistically, affecting many of the physiological processes of marine organisms (Gooding et al., 2009; Duarte et al., 2014). This highlights the importance of evaluating the combined effects of multiple environmental stressors (Darling and Cote, 2008; Pankhurst and Munday, 2011; Todgham and Stillman, 2013). Recent studies have shown that the effects of increased CO₂ could be modified by a rise in temperature (Gooding et al., 2009; Findlay et al., 2010; Navarro et al., 2016). It has been reported that elevated seawater CO₂ narrows the thermal tolerance window of an organism (Pörtner, 2008; Pörtner and Farrel, 2008). In this sense, Metzger et al. (2007) found that at elevated seawater CO₂ concentrations, the upper thermal tolerance limits were reduced by several degrees Celsius in crustaceans. Calcified and non-calcified species exposed to high pCO₂ are vulnerable to hypercapnia and acidosis (Melzner et al., 2009), demanding the reallocation of energy from fitness related traits (development, growth and reproduction) to acid-base regulatory processes in order to maintain homeostasis. These responses can also be exacerbated by an increase in the environmental temperature (Wang et al., 2018).

Sea lice are ectoparasitic copepods of the family Caligidae, have become one of the main problems for salmon farming worldwide, threatening the productivity of both salmon and trout farming (Burridge et al., 2014). In the future, this situation may be even more critical, with some authors suggesting that one of the impacts of climate change on aquaculture will be an increase in the incidence of diseases and parasites (Ruby and Ahilan, 2018). This ectoparasitic copepod attaches to the skin of its host to feed on mucus, generating wounds and therefore exposing fish to secondary infections, even leading to death at high infestation levels (Pike and Wadsworth, 1999; Costello, 2009; Valdés-Donoso et al., 2013; Oelckers et al., 2014). This in turn, increases production costs by extending the period to harvest and the handling time involved in the application of antiparasitic treatments (Bravo, 2003; Johnson et al., 2004; Costello, 2009; Agusti et al., 2016; Urbina et al., 2019), in addition to the treatment cost itself. In Chile, the main sea louse species is C. rogercresseyi (Boxshall and Bravo, 2000). The life cycle of this parasite involves eight stages, three non-feeding (lecithotrophic) free-living larval stages (2 nauplii and 1 copepodid) followed by 5 parasitic stages (4 chalimus and 1 adult) (González and Carvajal, 2003).

The present study aims to evaluate the combined effects of different pCO₂ levels and temperatures on hatching time, duration of the pelagic development, survival, size and respiration for the free-living larval stages of C. rogercresseyi (nauplii and copepodid stages). We hypothesize that increases in temperature and acidification of seawater will negatively impact the early pelagic stages of the ectoparasite C. rogercresseyi.