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Coral Reefs

, Volume 38, Issue 4, pp 721–730 | Cite as

Changes in abundance of fish-parasitic gnathiid isopods associated with warm-water bleaching events on the northern Great Barrier Reef

  • P. C. SikkelEmail author
  • M. A. Richardson
  • D. Sun
  • P. Narvaez
  • W. E. Feeney
  • A. S. Grutter
Report

Abstract

Mass coral bleaching events due to rising seawater temperatures are occurring with increasing frequency and are among the most conspicuous consequences of human-induced climate change. While bleaching events have clear impacts on the corals themselves, the impacts on other organisms and on the overall reef community are more difficult to assess. This is particularly true for parasitic organisms, which in spite of their high diversity and biomass are typically ignored in ecological monitoring studies. Here, we take advantage of long-term monitoring of host–parasite–cleaner interactions on experimental patch reefs to assess the effects of mass bleaching events on gnathiid isopod populations around Lizard Island, Great Barrier Reef. Compared with non-bleaching years, gnathiid abundance was consistently low during the warm-water period in bleaching years, but rebounded during the cooler months. This pattern is likely due to the interaction between the short-term negative impacts of thermal stress and declines in hosts on gnathiids, combined with the longer-term positive impacts of declines in cleaner wrasses and of increased dead coral on gnathiid abundance.

Keywords

Coral reefs Climate change Cleaning mutualism Fish parasites Predator–prey interaction Long-term monitoring 

Introduction

Mass coral bleaching events due to rising seawater temperatures are becoming increasingly frequent throughout the tropical Indo-Pacific and Western Atlantic (Glynn 1996; Hoegh-Guldberg 1999; Loya et al. 2001; Hughes et al. 2017). While bleaching events clearly impact corals, the impacts on other reef-associated organisms are more difficult to assess. This is attributable to two main factors. First, the location of bleaching events or even the probability of a bleaching event cannot be predicted with sufficient accuracy and sufficiently far in advance to plan pre-bleaching characterization of a site. Thus, proper BACI-type studies, and especially properly replicated studies (e.g., Underwood 1994), are generally not possible, leaving only comparisons of bleached and separate unbleached sites, after an event. This is particularly problematic if bleaching is widespread, as increasing distances between bleached and non-bleached sites decreases their comparability. Second, in cases where bleaching occurs at a site where pre-monitoring has occurred, the variables monitored may vary with, and depend on, the particular research teams.

While pre-bleaching monitoring efforts needed to assess post-bleaching consequences differ in the variables measured, there is some consistency in what is not measured. Parasitic organisms make up about 40% of the earth’s biodiversity (Hatcher and Dunn 2011), likely more in coral reef systems (e.g., Rohde 1976; Justine 2010; Justine et al. 2012), and can have high local biomass (Kuris et al. 2008). However, they are typically ignored in marine ecological monitoring studies and are represented in only about 5% of publications in marine journals (Poulin et al. 2014). Parasites can influence populations (e.g., Hatcher and Dunn 2011), food webs (e.g., Huxham et al. 1995; Thompson et al. 2005; Lafferty et al. 2006; Hatcher and Dunn 2011; Amundsen et al. 2009; Johnson et al. 2010), and thus community dynamics (e.g., Thomas et al. 1998; Mouritsen and Poulin 2002; Hatcher et al. 2006; Wood et al. 2007; Lafferty et al. 2008; Raffel et al. 2010; Hatcher and Dunn 2011). Neglect of this major component of biodiversity likely stems from their small size (“out of sight, out of mind”), and inconspicuous position on or within their hosts (Hatcher and Dunn 2011; Poulin et al. 2014), as well as lack of appropriate cross-training by marine ecologists.

Given the high diversity of parasites and their hosts, and their wide range of life history strategies, it is difficult to predict how any given environmental perturbation will impact them (Brooks and Hoberg 2007; Marcogliese 2001, 2008; Adlard et al. 2015). In the short term, bleaching events are characterized by unusually high water temperatures and changes in benthic substrate, associated with coral bleaching. In the long term, if warming events are protracted, more permanent changes in benthic community structure, associated with the death of corals, may occur. Parasites and hosts may be impacted in similar or different ways during the initial heating event, and impacts may change during the subsequent period. Understanding the effects of bleaching events on host–parasite interactions therefore requires pre- and post-bleaching monitoring of multiple parasite–host systems.

Juvenile gnathiid isopods are one of the most common ectoparasites of coral reef fishes and are perhaps best known for their role in cleaning symbioses, where they influence visitation in host fishes to cleaning stations (Grutter 2001; Côté and Molloy 2003; Sikkel et al. 2004) and are the main prey of cleanerfishes (Losey 1974; Grutter 1996; Arnal and Côté 2000). Gnathiids are born as small (approx. 1 mm) stage-1 juveniles. After feeding on a fish host, they become engorged with blood or fluid. They then molt into the second juvenile stage, feed again, and repeat the process a third time before metamorphosing into non-feeding adults. Adult females die within days after reproducing while males may persist for over a month after their last feeding (Smit and Davies 2004; Tanaka 2007). As generalists, gnathiids feed on a variety of host fishes (Jones et al. 2007; Coile and Sikkel 2013; Ota et al. 2012; Grutter et al. 2017). Unlike internal parasites such as nematodes and cestodes, and some ectoparasites such as copepods and monogeneans, gnathiids associate temporarily with their hosts, feeding on a different fish during each of their three juvenile stages. Because of this feeding strategy, which is similar to blood-feeding arthropods on land, gnathiids have been referred to as “ticks” or “mosquitoes” of the sea (e.g., Grutter et al. 2011) and may more appropriately be considered “micropredators” (Lafferty and Kuris 2002; Raffel et al. 2008).

In addition to their influence on host interactions with cleaners, gnathiids can have impacts on host physiology through reduced hematocrit (Jones and Grutter 2005), increased levels of corticosteroid stress hormones (Triki et al. 2016), and the creation of wounds that can lead to secondary infection (Honma and Chiba 1991). Gnathiids may also transmit blood-borne parasites (Smit and Davies 2004; Curtis et al. 2013). 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; Artim et al. 2015; Grutter et al. 2017; Sellers et al. 2019), and even sublethal infestation can impact performance (Sellers et al. 2019).

Given that gnathiids spend most of their lives in the benthos, must swim to attach to hosts, and must successfully feed and metamorphose three times in order to reproduce, warming per se, changes in benthic structure, and changes in fish communities that are associated with bleaching events may each impact their abundance in different ways. For example, increased temperature may impact rates of metamorphosis and swimming performance, but may can also impact the susceptibility of hosts to infestation. Changes in fish communities may impact host availability or abundance of gnathiid predators, and changes in substrate may impact the availability of suitable habitat (Artim and Sikkel 2013; Santos and Sikkel 2017).

In 2016, and again in 2017, the northern portion of the Great Barrier Reef (GBR) was impacted by a large-scale bleaching event that included the area around Lizard Island Research Station (Hughes et al. 2017). The presence of multiple long-term monitoring efforts provided the opportunity to assess the effects on multiple members of the coral reef community (e.g., Madin et al. 2018; Richardson et al. 2018). In this study, we take advantage of the only long-term monitoring of any marine parasite or micropredator in a coral reef system (Grutter et al. in press) to assess the impacts of the 2016–2017 Great Barrier Reef mass bleaching events on gnathiid isopod populations.

Materials and methods

Study location

This study was conducted on 12 patch reefs off Lizard Island Research Station, GBR (14°40′S, 145°28′E; Fig. S1), from July 2000 to October 2018; sampling after the first year was done opportunistically, with increased sampling done after the 2016 bleaching event and involving sampling over different seasons. These reefs were part of a cleaner wrasse (Labroides dimidiatus) removal study (Waldie et al. 2011) initiated in September 2000. For the present study, only the Lagoon site was used, and L. dimidiatus were removed from six reefs (removals), approximately every three months, and left undisturbed on six (control) reefs. Gnathiids were sampled during 21 trips. Removal Reef 4 at Lagoon (Fig. S1) was dropped after March 2008, due to a lone wandering male from neighboring Reef 5 (observed on three occasions in 2007 making short visits), but the samples were retained in analyses for the periods prior to this.

Field sampling

Gnathiid abundance was estimated using 1-m2 emergence traps (Jacoby and Greenwood 1988; Grutter et al. 2000; Chambers and Sikkel 2002). During all years, traps were set for three consecutive days at the Lagoon site, except for March 2008 and October 15 (2 d) and August 2017 (1 d). Traps were moved every 24 h. Sampling was conducted around the full moon (see Table S1 for dates) because gnathiid emergence at this site is highest at times of full and new moon (Grutter et al. 2000). When an additional site (Casuarina Beach) was sampled as part of another study (Grutter et al., in press), sampling order of each site was determined randomly (4 d before or after full moon, Table S1); when only the Lagoon reefs were sampled, this occurred after the full moon. In this study, only the Lagoon site was analyzed, with a maximum 180 samples per sampling trip.

We obtained both a day sample and a night sample from each trap within a 24-h period. Traps were positioned such that they would not cause damage to or be damaged by the reef. Thirty traps were positioned haphazardly across all reefs beginning at sunrise, with 2–3 reef−1 and the number depending on reef size. Sampling bottles were replaced with new ones at sunset each day to obtain daytime and nighttime samples. Samples from traps that were damaged or dislodged were excluded. Processing of samples followed Grutter et al. (2000).

The present study began in July 2000 and involved sampling initially at several month, then several year intervals until 2012, and then after the first recent (2016) GBR mass bleaching event, at approximately 3-month intervals. Exceptions to this protocol were a subset of samples in November 2017, one sample per reef for each day and each night (total n = 34) which were used for another study to identify the juvenile stage and species identity of gnathiids using host-feeding experiments; no counts were made of these samples. The sampling trips included the 2002 warm-water bleaching year, but not the 2006 year, and the 2016 and 2017 warm-water bleaching years (https://www.aims.gov.au/docs/research/climate-change/coral-bleaching/bleaching-events.html, Hughes et al. 2017).

Statistical analysis

Since July 2000 was the earliest sampling trip and cleanerfish had not yet been removed from removal reefs, this dataset was used as the baseline for the analysis of gnathiid abundance per trap. We tested for differences in gnathiid abundance (counts) using a generalized linear mixed effect model (GLMM), with cleaner presence, day/night, and sampling trip as categorical fixed effects; soak time (amount of time trap was deployed) to adjust for trap sampling duration as a covariate; and reef identity, area sampled, and sampling date as random factors. Since the data were very non-normal (Fig. 1), we used a negative binomial error distribution (with a log link function). To further explore the role of time and the potential effect of deviations from the norm in temperature, we conducted two additional analyses: one using time and the second using temperature difference (the difference between the ambient and long-term average, °C; for source and values, see Table S1) as a covariate instead of the fixed factor sampling trip in the above model. The GLMMs were done using the function “glmmadmb” in the package “glmmADMB” (Fournier et al. 2012; Skaug et al. 2016) and function “Anova” in the package “car” (Fox and Weisberg 2011), in R, version 3.2.3 (R Development Core Team 2016). We looked for data points with high influence (large residual and large Cook’s D statistic) by fitting multiple regression models to the data. Plots of residuals showed assumptions of analyses were met. Significant interactions were interpreted using plots of predicted values.
Fig. 1

Abundance of gnathiids. Boxplots of raw counts per trap among sampling trips (trip = sampling trip number), for day and night. Boxplots: center line = median, box = inner interquartiles, error bars = 90th and 10th percentiles, and circles = outliers

Results

Emergence trapping

A high percentage (83%) of samples contained gnathiids, with 35,720 gnathiids collected from 3338 samples. Gnathiid abundance trap−1 was highly variable (range 0–416, Fig. 1).

Gnathiid abundance patterns differed according to an interaction between day/night and sampling trip (GLMM: P < 0.0001, Table 1). This was due to numerous (nine) sampling trips differing from the day and night pattern of July 2000 (P < 0.05), with all significant coefficient estimates being positive indicating a greater abundance at night than day (Fig. 2a, Table S2). The higher night values ranged from 85 to 97% more gnathiids at night than the day per sampling trip (percentages calculated using backtransformed log values). Overall, ignoring sampling trip, pooled mean predicted log abundances for daytime and nighttime when backtransformed were 2 and 12 gnathiids trap−1, respectively, as shown in Fig. 2a. Ignoring day and night, the backtransformed predicted abundance ranged from 0.5 to 34 gnathiids trap−1 across sampling trips (Fig. 2b).
Table 1

Analysis of deviance table (Type II tests) showing model results for gnathiid abundance

Coefficient

df

χ 2

P

Cleaner

1

0.1042

0.7468

Daynight

1

10.2725

0.0013

Trip

20

134.5078

< 0.001

Soak time

1

2.5530

0.1100

Cleaner:daynight

1

0.6220

0.4303

Cleaner:trip

20

31.6778

0.0468

Daynight:tip

20

142.8137

< 0.001

Cleaner:daynight:trip

20

27.9527

0.1105

Probability values in bold are those mentioned in the text

Fig. 2

Abundance of gnathiids. Interaction plots with predicted mean log gnathiids trap−1 for a day (open symbol) and night (solid symbol) over time (i.e., trips or sampling trips) and b control (open symbol) and removal (solid symbol) cleaner presence treatments over time. Error bars are standard errors. Gray backgrounds represent bleaching years

Gnathiid abundance differed according to an interaction between cleaner presence treatment and sampling trip (GLMM: P = 0.04686, Table 1, Fig. 2b). The four significant differences, relative to pre-removal values in July 2000, involved more gnathiids present on removal reefs compared with controls in January 2001 (27%), December 2012 (27%), October 2016 (20%), and April 2017 (43%) (percentages calculated using backtransformed values, Fig. 2b, Table S2).

When sampling trip was converted to time and used as a covariate instead of as a fixed effect, the interaction between day/night and time was significant (GLMM: P = 0.0010 Table S3a). This was due to a decrease in gnathiids over time in the day, whereas in the night there was no such decrease (Fig. 2a, Table S3b). In contrast, when the temperature difference between daily ambient and long-term average was used as a covariate instead of time, it was not significant (GLMM: P = 0.3425, Table S4).

When examining patterns by month and year separately for day and night, to account for any potential seasonality, in the day samples there were no obvious patterns with bleaching, even without the possible outlier August 2017 which had very low gnathiid abundance values (Fig. 3a). By contrast, for night samples, when mean gnathiid abundance was always higher, there were fewer gnathiids collected from sampling trips during or just before (January 2002, 2017) and just after (April 2016, 2017), bleaching months (Fig. 3b). During bleaching years, gnathiid abundance from night samples rebounded during cooler months to levels that were comparable to, or higher than, those of non-bleaching years (Fig. 3b). Indeed, the highest levels ever recorded were during the October sampling trip during the 2016 bleaching year (Fig. 3b). However, in the non-bleaching year of 2018, after the two previous bleaching years, this “rebound” in the cooler months did not appear to occur, with levels appearing to decline slightly instead by October 2018 (Fig. 3b).
Fig. 3

Mean predicted log gnathiids per trap rearranged by month for each year separately for a day and b night. For standard errors, see Fig. 2. M = moderate temperature (0.44–0.92 °C) and H = high (1.1–1.44 °C) temperature increase between absolute and long-term average temperatures. Lines connect times sampled in same year. Lines and years in the legend that represent bleaching years are colored pink (i.e., 2002, 2016, 2017)

There was no consistent effect of cleaners over time. However, it is important to note that some reefs began to lose all cleaners in April 2016 (April 2016: one out of six reefs; July 2016: 4 out of 6 reefs). Despite this sudden decline in cleaners on these control reefs, no increase in gnathiids occurred there at this time. Eventually two reefs regained their cleaners (Jan 2017 Reef 5, February 2018 Reef 1, Fig. S1) and the remaining two regained their cleaners in October 2018 (Reefs 10 and Reef 13, Fig. S1). Thus, “cleaner” effects should be interpreted with caution.

Discussion

Because environmental factors can impact hosts, parasites, and the interaction between them (Lafferty and Kuris 1999; Mackenzie 1999; Sures et al. 1999; Williams and Mackenzie 2003; Sasal et al. 2007), understanding the impacts of extreme environmental changes on ecological communities requires an understanding of the impacts on parasites. We took advantage of our long-term monitoring of gnathiid isopods on experimental patch reefs to examine changes in gnathiid abundance associated with mass warm-water bleaching events around Lizard Island, GBR. To our knowledge, ours is the only research team to examine long-term population trends for any parasite or micropredator in coral reef systems and thus the first study to examine potential impacts of bleaching events. Given the widespread occurrence of these events, we were unable to compare bleached and unbleached reefs pre- and post-bleaching and were thus limited to a longitudinal comparison of our 12 patch reefs. Compared with non-bleaching years, the number of gnathiids collected in emergence traps was much lower during January and April sampling, which was the warm-water period during or shortly after the bleaching event. However, in subsequent samples during cooler months of these years, populations recovered to levels similar to those of non-bleaching years. This pattern occurred only during “night” samples that also include dawn and dusk periods—when more gnathiids are typically active (Grutter and Hendrikz 1999; Sikkel et al. 2006). Compared with bleaching years, population levels during non-bleaching years remained similar across seasons.

Decreases in abundance associated with above-normal water temperatures have been reported in other studies on small aquatic arthropods (e.g., Hogg and Williams 1996; reviewed by Przeslawski et al. 2008), and there are several non-mutually exclusive hypotheses that might explain the low levels of gnathiids observed in our study during summer in bleaching years. First, the high temperatures associated with bleaching may impair physiological performance. Tropical marine invertebrates have generally low tolerance for temperature fluctuations (Compton et al. 2007) and may suffer high mortality during warming events due to heat stress (Blidberg et al. 2000; Chan et al. 2006). In addition, high temperatures may impact rates of development (e.g., Reitzel et al. 2004; O’Connor et al. 2007). For gnathiids, this may mean that molting could begin before the blood meal is digested or that both digestion of the blood meal and metamorphosis are similarly expedited, meaning that gnathiid juveniles would need to find hosts sooner during their next feeding stage and have less time to do it before dying, due to increased metabolic demands and depleted energy reserves. Similarly, adults may utilize their final blood meal more quickly, leaving less time and energy for reproduction.

Bleaching events also appear to have significant impacts on host fishes (Booth and Beretta 2002; Wilson et al. 2006), attributable both to heat-induced mortality and to habitat degradation. Indeed, during the 2016 bleaching event, fish populations near our study reefs declined significantly (Triki et al. 2018), and fish assemblage structure was significantly altered (Richardson et al. 2018) through some combination of mortality and emigration. Given that gnathiids depend on host fishes for food, a significant decline in host fish populations and/or a change in the types of available host species could have significant negative impacts on gnathiid populations. The return of at least some fish species may contribute to the increase in gnathiid populations when waters cool, even when there is high coral mortality. The degree of “recovery” of gnathiid populations may further depend on the abundance of high quality host species versus smaller microcarnivores that may eat gnathiids (Artim et al. 2017).

Another factor that likely contributes to the recovery of gnathiid populations following bleaching events is the loss of live scleractinian corals. Corals can eat gnathiids, even when bleached, and even if gnathiids survive corals’ attempts to feed on them, they become covered in mucus from the coral (Artim and Sikkel 2013). Moreover, when given a choice, gnathiids actively avoid live corals, and fish hosts placed (in cages) on live coral are less likely to be infested with gnathiids than when they are placed on dead coral (Santos and Sikkel 2017). Given the strong negative impact of live corals on gnathiids, we expected that gnathiid abundance during the cooler months following high coral mortality would be consistently high, similar to the high October 2016 abundances observed. The lower number of fish hosts and/or the return of extreme warm water may have limited this. In addition and/or alternatively, coral cover prior to bleaching events may have been below the threshold necessary to effectively limit gnathiid populations.

Finally, the primary purpose of our monitoring efforts was a long-term experimental study on the effects of cleaner wrasses on gnathiid isopod populations and coral reef communities. Cleanerfish can consume hundreds of gnathiids daily (Grutter 1996), and they have been shown to reduce per capita infestation levels on host fish (Grutter et al. 2018). However, their impacts on gnathiid populations are less clear. This appears to be due to the dual effects of cleaner wrasse on clients. Cleaner wrasse depend on clients to provide food (mostly parasites) and remove parasites from them, and the presence of cleaner wrasse has been shown to locally enhance the abundance of fish, especially larger, highly mobile species (Bshary 2003; Waldie et al. 2011). Thus, mobile client fishes can both serve as local hosts for gnathiids (positive impact on gnathiids) that bring gnathiids to cleaners (negative impact on gnathiids), but also bring gnathiids to and from reefs through their diel movements (Sikkel et al. 2017). This could have positive (importing gnathiids) or negative (exporting gnathiids) impacts on local gnathiid abundance.

While half of our reefs had cleanerfish continually removed over years, during at least the most recent bleaching months, cleaner wrasse on most control reefs also disappeared. This disappearance corresponded with an overall decrease in fish abundance in the region (see above). It is therefore unclear whether cleanerfish drove changes in fish abundance, vice versa, or whether both were similarly impacted by thermal stress and either died or relocated. Triki et al. (2018) reported a 50% decrease in the abundance of “large” (> 10 cm) client species, but an 80% decrease in cleaner wrasse abundance near our study sites, resulting in an increase in the ratio of clients to cleaners. However, because the abundance of ectoparasites on clients is proportional to surface area, there was likely a decrease in available client surface area per cleanerfish biomass. Client removal experiments would be required to determine if a decrease in client biomass/surface area drives the departure of cleaner wrasses.

In summary, by including multiple bleaching and non-bleaching years during our monitoring, our data suggest a significant impact of bleaching events on the abundance of gnathiid isopods in shallow coral reef environments. While our data include multiple years pre and post for the earlier bleaching event, the occurrence of consecutive bleaching years in 2016–2017 resulted in only one (2018) post-bleaching year for these most recent events, which showed weak intra-annual variation similar to other non-bleaching periods. Given that the 2016 and 2017 bleaching events were particularly severe and widespread, “if recovery” of the broader coral reef community does occur, the expected recovery trajectory is long. This makes assessment of post-bleaching population trends for cryptic species like gnathiids more difficult. Given the expected increase but unpredictability of mass bleaching events, we therefore encourage more research teams to incorporate sampling of gnathiids, and other parasites and cryptic organisms in their monitoring efforts to increase our capacity for assessment of bleaching events on these organisms, which dominate coral reef biodiversity and have major impacts on coral reef community dynamics.

Notes

Acknowledgements

We are grateful to the staff of the Lizard Island Research Station for their years of support for our research program and to the many volunteers who have assisted with the collection and processing of samples. This study was supported by grants from the Australian Research Council and Sea World Research and Rescue Foundation, Australia (SWR/2/2012, TH Cribb, CI; D. Sun, Co-PI), and the US National Science Foundation (OCE-1536794, PC Sikkel, PI, A.S. Grutter, M. Dolan, Co-PI). Collecting and ethics approval were authorized by the Great Barrier Reef Marine Park Authority and The University of Queensland Animal Welfare Unit, respectively.

Compliance with ethical standards

Conflict of interest

The authors declare no conflicts of interest.

Supplementary material

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Supplementary material 1 (DOCX 1159 kb)

References

  1. Adlard RD, Miller TL, Smit NJ (2015) The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends in Parasitol 31:60–166CrossRefGoogle Scholar
  2. Amundsen PA, Lafferty KD, Knudsen R, Primicerio R, Klemetsen A, Kuris AM (2009) Food web topology and parasites in the pelagic zone of a subarctic lake. J Anim Ecol 78:563–572CrossRefPubMedGoogle Scholar
  3. Arnal C, Côté IM (2000) Diet of broadstripe cleaning gobies on a Barbadian reef. J Fish Biol 57:1075–1082CrossRefGoogle Scholar
  4. Artim JM, Sikkel PC (2013) Live coral repels a common reef–fish ectoparasite. Coral Reefs 32:487–494CrossRefGoogle Scholar
  5. Artim JM, Sellers JC, Sikkel PC (2015) Micropredation by gnathiid isopods on settlement–stage larval reef fish in the Eastern Caribbean Sea. Bull Mar Sci 91:479–487CrossRefGoogle Scholar
  6. Artim JM, Hook A, Grippo RS, Sikkel PC (2017) Predation on parasitic gnathiid isopods on coral reefs: a comparison of Caribbean cleaning gobies with non-cleaning microcarnivores. Coral Reefs 36:1213–1223CrossRefGoogle Scholar
  7. Blidberg E, Elfwing T, Planhnan P, Tedengren M (2000) Water temperature influences on physiological behaviour in three species of giant clams (Tridacnidae). In: Proceedings of the 9th international coral reef symposium, pp 561–565Google Scholar
  8. Booth DJ, Beretta GA (2002) Changes in a fish assemblage after a coral bleaching event. Mar Ecol Prog Ser 245:205–212CrossRefGoogle Scholar
  9. Bshary R (2003) The cleaner wrasse, Labroides dimidiatus, is a key organism for reef fish diversity at Ras Mohammed National Park, Egypt. J Anim Ecol 72:169–176CrossRefGoogle Scholar
  10. Brooks DR, Hoberg EP (2007) How will global climate change affect parasite–host assemblages? Trends in Parasitol 23:571–574CrossRefGoogle Scholar
  11. Chambers SD, Sikkel PC (2002) Diel emergence patterns of ecologically important, fish-parasitic, gnathiid isopod larvae on Caribbean coral reefs. Carib J Sci 38:37–43Google Scholar
  12. Chan BKK, Morritt D, De Pirro M, Leung KMY, Williams GA (2006) Summer mortality: effects on the distribution and abundance of the acorn barnacle Tetraclita japonica on tropical shores. Mar Ecol Prog Ser 328:195–204CrossRefGoogle Scholar
  13. Coile AM, Sikkel PC (2013) An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology 14:888–896CrossRefGoogle Scholar
  14. Compton TJ, Rijkenberg MJA, Drent J, Persma T (2007) Thermal tolerance ranges and climate variability: a comparison between bivalves from differing climates. J Exper Mar Biol Ecol 352:200–211CrossRefGoogle Scholar
  15. Côté IM, Molloy PP (2003) Temporal variation in cleanerfish and client behaviour: does it reflect ectoparasite availability? Ethology 109:487–499CrossRefGoogle Scholar
  16. Curtis LM, Grutter AS, Smit NJ, Davies Aj (2013) Gnathia aureamaculosa, a likely definitive host of Haemogregarina balistapi and potential vector for Haemogregarina bigemina between fishes of the Great Barrier Reef, Australia. Intl J Parasitol 43:361–370CrossRefGoogle Scholar
  17. Fournier DA, Skaug HJ, Ancheta J, Ianelli J, Magnusson A, Maunder M, Nielsen A, Sibert J (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249CrossRefGoogle Scholar
  18. Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand OaksGoogle Scholar
  19. Glynn PW (1996) Coral reef bleaching: facts, hypotheses and implications. Global Change Biol 2:495–509CrossRefGoogle Scholar
  20. Grutter AS (1996) Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser 130:61–70CrossRefGoogle Scholar
  21. Grutter AS (2001) Parasite infection rather than tactile stimulation is the proximate cause of cleaning behaviour in reef fish. Proc R Soc Lond 268:1361–1365CrossRefGoogle Scholar
  22. Grutter AS, Hendrikz J (1999) Diurnal variation in the abundance of juvenile parasitic gnathiid isopods on coral reef fish: implications for parasite-cleaner fish interactions. Coral Reefs 18:187–191CrossRefGoogle Scholar
  23. Grutter AS, Lester RJG, Greenwood J (2000) Emergence rates from the benthos of the parasitic juveniles of gnathiid isopods. Mar Ecol Prog Ser 207:123–127CrossRefGoogle Scholar
  24. Grutter AS, Pickering JL, McCallum H, McCormick MI (2008) Impact of micropredatory gnathiid isopods on young coral reef fishes. Coral Reefs 27:655–661CrossRefGoogle Scholar
  25. Grutter AS, Rumney JG, Sinclair-Taylor T, Waldie P, Franklin CE (2011) Fish mucous cocoons: the ‘mosquito nets’ of the sea. Biol Lett 7:292–294CrossRefPubMedGoogle Scholar
  26. Grutter AS, Blomberg SP, Fargher B, Kuris AM, McCormick MI, Warner RR (2017) Size-related mortality due to gnathiid isopod micropredation correlates with settlement size in coral reef fishes. Coral Reefs 36:549–559CrossRefGoogle Scholar
  27. Grutter AS, De Brauwer M, Bshary R, Cheney KL, Cribb TH, Madin EMP, McClure EC, Meekan MG, Sun D, Warner RR, Werminghausen J, Sikkel PC (2018) Parasite infestation increases on coral reefs without cleaner fish. Coral Reefs 37:15–24CrossRefGoogle Scholar
  28. Grutter AS, Blomberg SP, Box S, Bshary R, Ho O, Madin EMP, McClure EC, Meekan MG, Murphy JM, Richardson MA, Sikkel PC, Sims CA, Sun D, Warner RR (in press) Changes in local free-living parasite populations in response to cleaner manipulation over 12 years. OecologiaGoogle Scholar
  29. Hogg ID, Williams DD (1996) Response of stream invertebrates to a global-warming thermal regime: an ecosystem-level manipulation. Ecology 77:395–407CrossRefGoogle Scholar
  30. Hughes TP, Kerry JT, Álvarez-Noriega M, Álvarez-Romero JG, Anderson KD, Baird AH, Babcock RC, Beger M, Bellwood DR, Berkelmans R, Bridge TC (2017) Global warming and recurrent mass bleaching of corals. Nature 543(7645):373CrossRefPubMedGoogle Scholar
  31. Hatcher MJ, Dunn AM (2011) Parasites in ecological communities: from interactions to ecosystems. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  32. Hatcher MJ, Dick JT, Dunn AM (2006) How parasites affect interactions between competitors andpredators. Ecol Lett 9:1253–1271CrossRefPubMedGoogle Scholar
  33. Hayes PM, Smit NJ, Grutter AS, Davies AJ (2011) Unexpected response of a captive blackeye thicklip, Hemigymnus melapterus (Bloch), from Lizard Island, Australia, exposed to juvenile isopods Gnathia aureamaculosa Ferreira & Smit. J Fish Dis 34:563–566CrossRefPubMedGoogle Scholar
  34. Hoegh-Guldberg O (1999) Climate change, coral bleaching and the future of the world's coral reefs. Marine Freshwater Res 50:839–866CrossRefGoogle Scholar
  35. Honma Y, Chiba A (1991) Pathological changes in the branchial chamber wall of stingrays, Dasyatis spp., associated with the presence of juvenile gnathiids (Isopoda, Crustacea). Fish Pathol 26:9–16CrossRefGoogle Scholar
  36. Huxham M, Raffaelli D, Pike A (1995) Parasites and food web patterns. J Anim Ecol 64:168–176.  https://doi.org/10.2307/5752 CrossRefGoogle Scholar
  37. Jacoby CA, Greenwood JG (1988) Spatial, temporal, and behavioral patterns in emergence of zooplankton in the lagoon of Heron Reef, Great Barrier Reef, Australia. Marine Biol 97:309–328CrossRefGoogle Scholar
  38. Johnson PT, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371.  https://doi.org/10.1016/j.tree.2010.01.005 CrossRefPubMedGoogle Scholar
  39. Jones CM, Grutter AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive Hemigymnus melapterus (Bloch) (Pisces: Labridae) on the Great Barrier Reef. J Fish Biol 66:860–864CrossRefGoogle Scholar
  40. Jones CM, Nagel L, Hughes GL, Cribb TH, Grutter AS (2007) Host specificity of two species of Gnathia (Isopoda) determined by DNA sequencing blood meals. Intl J Parasitol 37:927–935CrossRefGoogle Scholar
  41. Justine JL (2010) Parasites of coral reef fish: how much do we know? With a bibliography of fish parasites in New Caledonia. Belgian J Zool 140:155–190Google Scholar
  42. Justine JL, Beveridge I, Boxshall GA, Bray RA, Miller TL, Moravec F, Trilles JP, Whittington ID (2012) An annotated list of fish parasites (Isopoda, Copepoda, Monogenea, Digenea, Cestoda, Nematoda) collected from Snappers and Bream (Lutjanidae, Nemipteridae, Caesionidae) in New Caledonia confirms high parasite biodiversity on coral reef fish. Aquat Biosyst 8:22CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kuris AM, Hechinger RF, Shaw JC et al (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518CrossRefPubMedGoogle Scholar
  44. Lafferty KD, Kuris AM (1999) How environmental stress affects the impacts of parasites. Limnol Oceanog 44:925–931CrossRefGoogle Scholar
  45. Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513.  https://doi.org/10.1016/S0169-5347(02)02615-0 CrossRefGoogle Scholar
  46. Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci 103:11211–11216CrossRefPubMedGoogle Scholar
  47. Lafferty KD, Allesina S, Arim M et al (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11:533–546CrossRefPubMedPubMedCentralGoogle Scholar
  48. Losey GS (1974) Cleaning symbiosis in Puerto Rico with comparison to the tropical Pacific. Copeia 1974:960–970CrossRefGoogle Scholar
  49. Loya Y, Sakai K, Yamazato K, Nakano Y, Sambali H, van Woesik R (2001) Coral bleaching: the winners and the losers. Ecol Letters 4:122–131CrossRefGoogle Scholar
  50. Mackenzie K (1999) Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Poll Bull 38:955–959CrossRefGoogle Scholar
  51. Madin JS, Baird AH, Bridge T, Connolly SR, Zawada K, Dornelas M (2018) Cumulative effects of cyclonesand bleaching on coral cover and species richness at Lizard Island. Mar Ecol Prog Ser 604:263–268CrossRefGoogle Scholar
  52. Marcogliese DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Can J Zool 79:1331–1352CrossRefGoogle Scholar
  53. Marcogliese DJ (2008) The impact of climate change on the parasites and infectious diseases of aquatic animals. Rev Sci Tech 27:467–484CrossRefPubMedGoogle Scholar
  54. Mouritsen KN, Poulin R (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:101–117.  https://doi.org/10.1017/S0031182002001476 CrossRefGoogle Scholar
  55. Mugridge RER, Stallybrass HG (1983) A mortality of eels, Anguilla anguilla L., attributed to Gnathiidae. J Fish Disease 6:81–82CrossRefGoogle Scholar
  56. O’Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, Kinlan BP, Weiss JM (2007) Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. Proc Nat Acad Sci US 104:1266–1271CrossRefGoogle Scholar
  57. Ota Y, Hoshino O, Hirose M, Tanaka K, Hirose E (2012) Third–stage larva shifts host fish from teleost to elasmobranch in the temporary parasitic isopod, Gnathia trimaculata (Crustacea; Gnathiidae). Mar Biol 159:2333–2347CrossRefGoogle Scholar
  58. Przeslawski R, Ahyong S, Byrne M, Woerheide G, Hutchings PAT (2008) Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Global Change Biol 14:2773–2795CrossRefGoogle Scholar
  59. Poulin R, Blasco-Costa I, Randhawa HS (2014) Integrating parasitology and marine ecology: seven challenges towards greater synergy. J Sea Res 113:3–10.  https://doi.org/10.1016/j.seares.2014.10.019 CrossRefGoogle Scholar
  60. R Development Core Team (2016) R: a language and environment for statistical computing. R foundation for statistical computing, ViennaGoogle Scholar
  61. Raffel TR, Martin LB, Rohr JR (2008) Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol 23:610–618.  https://doi.org/10.1016/j.tree.2008.06.015 CrossRefPubMedGoogle Scholar
  62. Raffel TR, Hoverman JT, Halstead NT, Michel PJ, Rohr JR (2010) Parasitism in a community context: trait-mediated interactions with competition and predation. Ecology 9:1900–1907.  https://doi.org/10.1890/09-1697 CrossRefGoogle Scholar
  63. Reitzel AM, Miner BG, McEdward LR (2004) Relationships between spawning date and larval development time for benthic marine invertebrates: a modelling approach. Mar Ecol Prog Ser 280:13–23CrossRefGoogle Scholar
  64. Richardson LE, Graham NA, Pratchett MS, Eurich JG, Hoey AS (2018) Mass coral bleaching causes biotic homogenization of reef fish assemblages. Global Change Biol 24:3117–3129CrossRefGoogle Scholar
  65. Rohde K (1976) Species diversity of parasites on the Great Barrier Reef. Parasitol Res 50:93–94Google Scholar
  66. Santos TRN, Sikkel PC (2017) Habitat associations of fish-parasitic gnathiid isopods in a shallow reef system in the central Philippines. Mar Biodiv.  https://doi.org/10.1007/s12526-017-0756-6 CrossRefGoogle Scholar
  67. Sasal P, Mouillot D, Fichez R, Chifflet S, Kulbicki M (2007) The use of fish parasites as biological indicators of anthropogenic influences in coral-reef lagoons: a case study of Apogonidae parasites in New-Caledonia. Marine Poll Bull 54:1697–1706CrossRefGoogle Scholar
  68. Sellers JC, Holstein DM, Botha TI, Sikkel PC (2019) Lethal and sublethal impacts of a micropredator on post-settlement Caribbean reef fishes. Oecologia 189:293–305CrossRefPubMedGoogle Scholar
  69. Sikkel PC, Cheney KL, Côté IM (2004) In situ evidence for ectoparasites as a proximate cause of cleaning interactions in marine reef fish. Anim Behav 68:241–247CrossRefGoogle Scholar
  70. Sikkel PC, Schaumburg CS, Mathenia JK (2006) Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs 25:683–689CrossRefGoogle Scholar
  71. Sikkel PC, Welicky RL, Artim JM, McCammon AM, Sellers JC, Coile AM, Jenkins WG (2017) Nocturnal migration reduces exposure to micropredation in a coral reef fish. Bull Mar Sci 93:475–489CrossRefGoogle Scholar
  72. Skaug H, Fournier D, Bolker B, Magnusson A, Nielsen A (2016) Generalized Linear Mixed Models using ‘AD Model Builder’. R package version 0.8.3.3 2016-01-19Google Scholar
  73. Smit NJ, Davies AJ (2004) The curious life–style of the parasitic stages of gnathiid isopods. Adv Parasitol 58:289–391CrossRefPubMedGoogle Scholar
  74. Sures B, Siddall R, Taraschewski H (1999) Parasites as accumulation indicators of heavy metal pollution. Parasitol Today 15:16–21CrossRefPubMedGoogle Scholar
  75. Tanaka K (2007) Life history of gnathiid isopods–current knowledge and future directions. Plankton Benthos Res 2:1–11CrossRefGoogle Scholar
  76. Thomas F, Renaud F, de Meeûs T, Poulin R (1998) Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proc R Soc Lond B 265:1091–1096CrossRefGoogle Scholar
  77. Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85.  https://doi.org/10.1111/j.1365-2656.2004.00899.x CrossRefGoogle Scholar
  78. Triki Z, Grutter AS, Bshary R, Ros AF (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Mar Biol 163:187.  https://doi.org/10.1007/s00227-016-2959-y CrossRefGoogle Scholar
  79. Triki Z, Wismer S, Levorato E, Bshary R (2018) A decrease in the abundance and strategic sophistication of cleaner fish after environmental perturbations. Global Change Biol 24:481–489CrossRefGoogle Scholar
  80. Underwood AJ (1994) On beyond BACI: sampling designs that might reliably detect environmental disturbances. Ecol. App. 4:3–15CrossRefGoogle Scholar
  81. Waldie PA, Blomberg SP, Cheney KL, Goldizen AW, Grutter AS (2011) Long-term effects of the cleaner fish Labroides dimidiatus on coral reef fish communities. PLoS one 6:e21201CrossRefPubMedPubMedCentralGoogle Scholar
  82. Williams HH, MacKenzie K (2003) Marine parasites as pollution indicators: an update. Parasitology 126:S27–S41CrossRefPubMedGoogle Scholar
  83. Wilson SK, Graham NA, Pratchett MS, Jones GP, Polunin NV (2006) Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk or resilient? Global Change Biol. 12:2220–2234CrossRefGoogle Scholar
  84. Wood CL, Byers JE, Cottingham KL, Altman I, Donahue MJ, Blakeslee AM (2007) Parasites alter community structure. Proc Natl Acad Sci 104:9335–9339CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Biological Sciences and Environmental Sciences ProgramArkansas State UniversityState UniversityUSA
  2. 2.Water Research Group, Unit for Environmental Sciences and ManagementNorth-West UniversityPotchefstroomSouth Africa
  3. 3.School of Biological SciencesThe University of QueenslandSt. LuciaAustralia
  4. 4.ARC Centre of Excellence for Coral Reef StudiesJames Cook UniversityTownsvilleAustralia
  5. 5.Centre for Sustainable Tropical Fisheries and Aquaculture, College of Science and EngineeringJames Cook UniversityTownsvilleAustralia
  6. 6.Environmental Futures Research InstituteGriffith UniversityNathanAustralia

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