1. Introduction
Human-induced environmental changes currently represent the single greatest threat to global diversity. Earth’s atmospheric concentration of carbon dioxide (CO
2) has been increasing at an unparalleled rate. Currently, 30% of the anthropologically emitted CO
2 is being dissolved into the ocean, which has decreased seawater pH by 0.1 units during the last decade [
1]. When CO
2 is dissolved in seawater, CO
2 concentration increases and combines with water to produce carbonic acid (H
2CO
3); this dissociates into bicarbonate (HCO
3-) and hydrogen ions decreasing seawater pH. The increased concentration of hydrogen ions can also interact with carbonate ions (CO
32-) to form more bicarbonate, reducing the saturation of seawater aragonite and calcite, crucial for shells and skeletons of marine organisms. This phenomenon, known as ocean acidification (OA), is projected to decrease seawater pH between 0.14–0.42 units by the end of this century [
1,
2].
Different biological responses to OA have been observed across multiple taxa, with sensitivity varying according to the measured trait, life stage, species and exposure duration [
3]. OA is known to affect growth, survival, reproduction and behaviour of multiple species. In coral reefs, calcification is one of the most critical functions to be affected by OA. Lower calcification rates in corals under OA can result in slower coral growth and more fragile structures, making corals more susceptible to disturbances [
4]. OA can also lead to the reduced abundance of crustose coralline algae, crucial to larval recruitment of invertebrates [
5] and reduce zooplankton community biomass [
6].
Although coral reef fish can regulate their acid-balance [
7], coral reef fishes have been suggested to be susceptible to physiological and behavioural alterations under OA [
7,
8,
9], yet, recent studies have also documented low or no effect of OA on fish behaviour [
10,
11,
12], suggesting at least variability in fish behavioural responses to OA. During cleaning interactions, cleaner fishes inspect the body of their clients for ectoparasites, dead tissue and mucus [
13]. Recently, Paula et al. (2019) [
14] described a loss in motivation in cleaner wrasse
Labroides dimidiatus (the most abundant cleaner fish species in the Indo-Pacific [
15]) to interact with a client reef species.
Gnathiid isopods (family: Gnathiidae) are the most common ectoparasites found on coral reef fishes [
16], and they can lower blood volume of their host, cause tissue damage, transmit blood-borne protozoan parasites and, in large numbers, can even cause death to adult fish [
17,
18]. Fish larvae and juveniles are especially vulnerable to the effects of ectoparasite infection, as they are small relative to the parasite, and can experience reduced performance and even mortality when infected [
18,
19]. Cleaning interactions can significantly lower the gnathiid loads on fish [
20] and can indirectly affect gnathiid populations [
21]. When not feeding on hosts, these ectoparasites are part of the demersal zooplankton community [
22].
Nevertheless, despite the effects of OA on cleaner fish motivation and the ecological relevance of gnathiid ectoparasites, until now, the effect of OA on gnathiids has not been tested. To understand the effects of OA on gnathiids, we tested whether the survival rate of a cultured gnathiid species,
Gnathia aureamaculosa, is altered when exposed to projected OA conditions (~980 μatm pCO
2, RCP8.0 2100, in IPCC 2013 [
1]).
4. Discussion
OA has the potential to reduce the abundance of demersal zooplankton that reside in tropical coral reefs [
6]. However, in our study, we did not observe an effect of OA on the short-term survival of the gnathiid
G. aureamaculosa, an organism that forms part of the tropical reef demersal zooplankton community. Since all gnathiids considered here were not fed (i.e., no potential host was provided), all gnathiids reached death during this study most likely due to starvation. Our results indicate that, although survival was dependent on larval stage and on headwidth within a larval stage, gnathiid survival was not significantly affected by OA. Overall, there was a non-significant tendency for third stages to survive longer, with 50% of individuals surviving after 12 to 13 days, compared with 7 and 9 days for stage one and two, respectively (
Figure 1). The gnathiid survival increase with age might be related to different resource allocation, as, for example, third stage gnathiids have to allocate resources to prepare reproductive organs [
25]. Moreover, gnathiid survival increases with size and varies with age (AS Grutter personal communication), however this response could have varied if gnathiids were fed.
Determining which species are sensitive to OA is crucial to determine the impacts of OA on ecosystem function [
30,
31]. Previous studies have shown that extreme OA (2380 μatm pCO
2) has little to no impact on the survival of non-calcifying zooplankton species, such as copepods [
32]. However, in a naturally acidified reef, Smith et al. (2016) [
6] observed a loss of reef-associated demersal zooplankton abundance, including zooplankton from the Order Isopoda, without any shift in diversity. The authors suggested that although this loss could be driven by: (i) an indirect effect of physiological or behavioural impacts of OA, and (ii) reduced habitat complexity (i.e., higher abundance of branching corals at control sites, compared to a domination of massive bouldering corals in high CO
2 sites). Although, in the case of gnathiids, loss of habitat complexity can be beneficial since a previous study demonstrated that gnathiids (
Gnathia marleyi) prefer less complex habitats [
33].
During our study, gnathiids were isolated in small vials and left to starve. We cannot ignore that potential OA effects on gnathiid physiology, digestion or behaviour (e.g., host detection and attachment success) could have indirect effects on gnathiid survival. OA can induce alterations of stomach pH in marine invertebrates leading to decreased digestive efficiencies [
34]. Other studies also showed that host-parasite dynamics can vary with OA. Namely, increased infection rates of trematodes (
Maritrema novaezealandensis) in amphipods have been described under severe acidification (pH 7.4 ~1980 pCO
2, 2300 scenario) [
35]. Contrarily, no effects were observed in infection rates of
Perkinsus marinus in
Crassostrea virginica [
36]. Moreover, exposure to ocean acidification decreased cercarial survival of four parasite species (
M. novazelandensis,
Philophthalmus sp.,
Parorchis sp., and
Galactosum sp.) [
37]. Thus, further studies are necessary to understand hosts’ susceptibility to gnathiids and the attachment success of gnathiids onto hosts, as well as the biological interactions in other parasite systems under OA.
Environmental perturbations, such as bleaching and cyclones, can lower cleaner fish abundance considerably [
38] and OA has the potential to disrupt cleaning interactions [
14]. Such perturbations could lead to disruptions in cleaners’ control of gnathiid abundances [
39]. Our results, indicating an apparent tolerance of these fish ectoparasites to OA, suggest that a potential cascading impact of OA on the cleaning symbiosis may include the continued need for cleaners’ parasite removal services in clients under projected OA conditions.