Micropredation by Gnathiid Isopods on Settlement-Stage Reef Fish in The

Home , Gnathia marleyi, Haemulon flavolineatum, Labrisomid

Bull Mar Sci. 91(4):479–487. 2015 coral reef paper http://dx.doi.org/10.5343/bms.2015.1023

Micropredation by gnathiid isopods on settlement- stage reef fish in the eastern Caribbean Sea

1 Department of Biological John M Artim 1 Sciences and Environmental 2 Sciences Program, Arkansas Joseph C Sellers State University, State Paul C Sikkel 1, 3 * University, Arkansas 72467. 2 Center for Marine and Environmental Studies, University of the Virgin Islands, ABSTRACT.—The transition from a planktonic larval 2 Brewers Bay, St. Thomas, USVI stage to a benthic or demersal juvenile stage is a crucial event 00802. in the life history of coral reef fishes, and recruitment success has a strong influence on reef-fish population size. Post- 3 Water Research Group, Unit for Environmental Sciences settlement predation is thought to limit recruitment success. and Management, North-West Most studies on post-settlement predation have focused on University, Potchefstroom 2520, piscivorous reef fishes. However, recent studies in the tropical South Africa. Pacific Ocean suggest that blood-feeding ectoparasites may * Corresponding author email: also be an important source of predation. Here we provide , phone: further evidence that a gnathiid ectoparasite is capable of 870-972-3296, fax: 870-972-2638. such “micropredation” on settlement-stage fish in the eastern Caribbean Sea. On 12 occasions in May–August, 2014 and 2015, during plankton light-trap recovery, we observed post- settlement fishes from the families Apogonidae, Bothidae, Gobiidae, Labrisomidae, and Tripterygiidae with attached ectoparasitic juvenile gnathiid isopods. In one laboratory experiment in which 10 settlement-stage French grunt, Haemulon flavolineatum (Desmarest, 1823), were fed upon by an average of one gnathiid per fish, all fish died compared to none in the control group. In a subsequent experiment in which individual settlement-stage French grunt were exposed to 0–3 gnathiids each, all 50 fish that were fed upon by at least one gnathiid died, compared with only one of 78 that were not fed on by any gnathiids. Combined with observations on damselfishes from the Pacific Ocean, these findings suggest that gnathiids are capable of micropredation on larval fish at time of reef settlement and that micropredation should be Date Submitted: 8 April, 2015. Date Accepted: 23 September, 2015. further evaluated as a factor affecting success of settlement Available Online: 19 October, 2015. and thus recruitment success of coral reef fishes.

With few exceptions, the early life history of coral reef fishes consists of a pelagic larval stage, followed by a benthic or demersal juvenile stage. The transition between habitats and life history stages is associated with significant changes in morphology and exposure to reef-based predators. Predation on early post-settlement stages can have significant effects on recruitment to and therefore the density and dynamics of reef-fish populations (e.g., Carr and Hixon 1995, Forrester and Steele 2004, reviewed by Hixon 2015). The source of predation has generally been considered to be small piscivorous fishes. However, recent studies in the tropical Pacific Ocean suggest that

Bulletin of Marine Science 479 OA © 2015 Rosenstiel School of Marine & Atmospheric Science of the University of Miami Open access content 480 Bulletin of Marine Science. Vol 91, No 4. 2015 ectoparasites may sometimes function as “micropredators” (Raffel et al. 2008) and thus contribute to mortality of recently settled reef fishes (Grutter et al. 2008, Jones and Grutter 2008, Penfold et al. 2008). Gnathiid isopods are small (1–3 mm) protelean parasites that feed on fish blood during each of three larval stages and live in the substratum between feedings. Thus, they are ecologically similar to terrestrial haematophagous arthropods, such as ticks (Ixodoidea) and fleas (Siphonoptera). After the third feeding, gnathiids metamor- phose into non-feeding adults, reproduce, and die (Smit and Davies 2004, Tanaka 2007). Although gnathiids can be found in the benthos from polar regions to the equa- tor (e.g., Klitgaard 1997), they have been reported mostly in warm temperate and tropical waters, and are one of the most common ectoparasites of coral reef fishes (Grutter 1994, Grutter and Poulin 1998), where they infest a wide range of host species (Arnal et al. 2001, Ferreira et al 2009, Coile and Sikkel 2013). Though small in size, in sufficient abundance gnathiids have been shown to lower the hosts’ blood volume (Jones and Grutter 2005), cause serious tissue damage, and even kill adult host fish (Bunkley-Williams and Williams 1998). Therefore, even in small numbers, they have the potential to damage or kill newly settled reef fishes, especially given that settlement in reef fishes typically occurs at night (e.g., Stobutzki and Bellwood 1998), when the most and largest gnathiids are active (Grutter 1999, Sikkel et al. 2006, 2009). However, the fact that these events occur at night, that gnathiids remain on hosts only during a brief feeding period, and have the potential to kill small hosts, also makes it difficult to document micropredation by gnathiids in the field. Here we provide the first report of gnathiid isopods infesting settlement-stage reef fishes in the tropical Atlantic Ocean, extend the list of affected fish taxa with five additional families, and provide further experimental evidence that as few as one gnathiid can kill settlement-stage fish.

Methods

Field Observations.—Lighted plankton traps (Fig. 1) similar to those used in studies of gnathiids at sites on the Great Barrier Reef (Jones and Grutter 2007) were set between May and August 2014 and 2015 in Greater Lameshur Bay, St. John, US Virgin Islands (18.31502°, −64.722904°); a bay dominated by a mix of rocky reef, live and dead Orbicella annularis (Ellis and Solander, 1786) coral, sand, and seagrass. These traps are constructed of PVC and use a LED marker light as a light source and translucent white plastic funnels as one-way entry points. The LED marker light is activated and placed within the trap so that the entry funnel is illuminated. Traps were set 2–3 hrs prior to sunset and were retrieved either 3 hrs after sunset that evening, or 3 hrs post-sunrise the next day. The contents of the traps were filtered through 160-μm plankton mesh and placed in seawater in one or more petri dishes; any gnathiids found were removed, counted, and photographed for another study. The traps attracted and collected a wide range of small organisms, including some settlement-stage fishes. For the remainder of the 2014 field season and all of the 2015 season, when we found settlement-stage fish in a sample, the number of attached gnathiids was noted and the fish with attached gnathiids were placed in a separate petri dish for observation or, in one case noted below, the fish and gnathiid were placed in a larger container overnight. In another case, a settlement stage Acanthurus sp. Artim et al.: Gnathiid micropredation on larval reef fish 481

Figure 1. Light trap used to collect gnathiid isopods and settlement-stage reef fishes. was collected from the water column at night and exposed to three gnathiids in the laboratory overnight. Fish standard length (SL) and key major-axis dimensions for attached gnathiids were measured from digital photographs using ImageJ (Abràmoff et al. 2004). Major- axis dimensions for gnathiids and for their blood and plasma bolus were used to estimate gnathiid juvenile stage and volume of blood and plasma removed by the parasite. Blood and plasma volume was approximated by an ellipsoid whose two mi- nor radii are identical, allowing for estimates from head-on 2-D photographic views. Fish were identified at least to family from the photographic images. Laboratory Experiments.—To further assess whether small numbers of gnathiids are capable of causing mortality in settlement-stage fish, we conducted two experiments using newly settled French grunt, Haemulon flavolineatum (Desmarest, 1823) collected from Brewers Bay, St. Thomas, US Virgin Islands (18.33053°, −64.961472°). Fish, ranging from 7 to 15 mm total length (TL), were collected by escorting them into a plastic container. In the first experiment, 10 fish were randomly assigned to gnathiid-exposed or control treatment. For the former, a total of 48 stage-3 gnathiid zuphea were added to the 1.5-L aerated container of seawater at dusk, and remained with the fish overnight. No gnathiids were added to the control container. The follow- ing day, the number of fish that died and number of gnathiids that fed were recorded. In the second experiment, individual fish were randomly assigned to 0 n( = 32), 1 (n = 35), 2 (n = 33), or 3 (n = 30) gnathiids placed in 0.40-L containers with a single fish. As before, fish were held overnight and the number of fish that died and number of gnathiids that fed were recorded. For both experiments, Chi-squared analyses were performed to test for an effect of exposure to gnathiids on fish mortality rates. 482 Bulletin of Marine Science. Vol 91, No 4. 2015

Table 1. Summary of field observations on gnathiid micropredation on settlement-stage reef fish. Fish fluid volumes and gnathiid blood meal volumes are estimates based on size measurements.

Fork length Fish fluid Total blood meal Body fluid Date observed Family in mm volume in μl volume in μl extracted Fatal May 2014 Labrisomidae 10.2 0.96 0.37 38.7% Yes July 2014 Bothidae 14.1 2.42 0.06 2.5% Yes May 2015 Acanthuridae 25.0 16.13 1.09 6.7% No June 2015 Gobiidae 16.9 4.45 0.36 1.5% Yes June 2015 Gobiidae 14.9 5.37 0.14 0.5% No June 2015 Gobiidae 6.8 0.34 0.09 5.1% Yes July 2015 Apogonidae 12.8 6.66 0.21 0.6% No July 2015 Gobiidae 8.3 1.19 0.68 10.8% Yes July 2015 Bothidae 20.2 14.99 0.54 0.7% Frozen July 2015 Triptigeridae 20.1 14.72 0.04 0.0% Frozen July 2015 Labrisomidae 21.9 18.18 0.06 0.1% Frozen July 2015 Gobiidae 11.3 1.10 0.17 2.9% Frozen

Results

Field Observations.—A summary of field observations is presented in Table 1. In three instances in 2014, settlement-stage fish removed from traps were infested with gnathiids. The first occasion, in May 2014, was a labrisomid blennyStarksia ( sp.; 10.2 mm FL) with five gnathiids, Gnathia marleyi Farquharson, Smit & Sikkel, 2012 (Farquharson et al. 2012) attached. This fish and four of the five gnathiids can be seen in Figure 2A and 2B. The five gnathiids on this fish varied in size from 1.53 to 2.26 mm and extracted an estimated 0.37 μl of blood and plasma volume. Using the blood-volume to body-mass ratio for fish of 0.022 L kg−1 (Schmidt-Nielsen 1997), this 5.01 mg fish had approximately 0.11 μl of blood. Similarly, the whole-body extracellular fluid volume can be estimated using the mean of the measurements Olson reported for reef-dwelling species—0.189 L kg−1 (Olson 1992). For this fish, the ap- proximation yields a value of 0.95 μl of fluid. The fluids extracted by gnathiids can be seen through the gnathiid carapace in the images in Figure 2. These fluids clearly include some whole blood but also appear to include plasma or other extracellular fluid. Our estimate of 0.37 μl of extracted fluids is approximately 39% of the estimated extracellular fluid volume of this fish, making rapid fluid loss a plausible cause of death. One hour of the gnathiid attack on this labrasomid blenny was recorded on video and a short excerpt of the recording, including the point at which the fish’s respiration ceases, is included as Supplementary Online Video 1. The second occasion occurred in June 2014 with the appearance of a larval fish with a single gnathiid attached. This fish was retained in 500 ml of filtered seawater along with the attached gnathiid. The fish was still alive 12 hrs later. The image file for this observation was lost—no size measurements or fish species identification are available. The third occasion occurred in July 2014 with the appearance of a flounder (Bothus sp.; 14.1 mm FL) with a single gnathiid, approximately 2.13 mm TL. This fish lar- va and gnathiid can be seen in the photos in Figure 2C and 2D. From size measurements, this appeared to be a second-stage juvenile gnathiid that had extracted approximately 0.06 μl of blood and fluid volume. The total volume of this fish, as Artim et al.: Gnathiid micropredation on larval reef fish 483

Figure 2. Microphotographs of the larval fish and gnathiids attached to them. (A)Starksia sp. fish larvae with four of the five attached feeding gnathiid larvae with the fifth gnathiid attached on the opposite side of the fish. (B) Closeup of gnathiids attached to the ventral surface of the Starksia sp. larvae. (C) Bothus sp. fish larvae with the attached gnathiid. (D) Close-up of the gnathiid at- tachment on this Bothus sp. fish. measured from photographs, is 12.8 μl. Using the same constants as for the first fish above, we estimate a blood volume of 0.28 μl and an extracellular fluid volume of 2.42 μl. Thus, the 0.06 μl of extracted blood and plasma represent 2.5% of this fish’s estimated extracellular fluid volume—a considerably larger proportion than when a similar-sized gnathiid feeds on an adult fish. In 2015, settlement-stage fish along with gnathiids were found in 52 traps with gnathiids attached to fish in nine instances. The nine fish larvae with attached gnathiids included members of the families Gobiidae (n = 5), Apogonidae (n = 1), Bothidae (n = 1), Labrisomidae (n = 1), and Triptyrigiidae (n = 1). In four cases, samples were frozen upon retrieval and thus all contents were dead before the attached gnathiids were discovered. However, in three of the remaining five cases, the fish was found dead with a single gnathiid attached. The relatively large (25 mm) settlement-stage Acanthurus sp. was fed on by two gnathiids and survived. 484 Bulletin of Marine Science. Vol 91, No 4. 2015

Table 2. Summary of results of laboratory experiment 2 on gnathiid micropredation on settlement- stage reef fish (see text for details). Effects of exposure of individual recently settled French grunt (Haemulon flavolineatum; 7–15 mm) to 0–3 third stage gnathiid isopods (Gnathia marleyi).

Gnathiids per fish Percentage of fish infested Mortality of infested fish Overall mortality 0 0.00% na 3.33% 1 57.14% 100.00% 57.14% 2 45.45% 100.00% 45.45% 3 50.00% 100.00% 50.00%

In total, 158 settlement stage fish were collected from traps that also contained gnathiids. Among these fish, 12 were observed with attached gnathiids, and five of these died with the gnathiid attached (Table 1). Laboratory Experiments.—The results of both experiments are summarized in Table 2. In the first experiment, where a group of 10 fish was exposed to 48 gnathiids, 12 gnathiids fed on the 10 fish (approximately 1 per fish) and all fish died. In -con trast, none of the 10 control fish died. This is significantly different than expected if mortality rates were independent of gnathiid exposure (χ2 = 11.16, df = 1, P = 0.039). In the second experiment, where individual fish were exposed to 0–3 gnathiids, there was a significant difference in mortality among treatments. Only 3.33% of fish in the control treatment (0 gnathiids) died, compared to 45.45%–57.14% of fish exposed to gnathiids (χ2 = 22.78, df = 3, P < 0.001). When the control group was removed from the analysis, the difference among the remaining three treatments (1, 2, or 3 gnathiids) was no longer significant (χ2 = 0.947, df = 2, P = 0.623). Moreover, within the three treatments, in which fish were exposed to gnathiids, 100% of fish mortality was attributable to gnathiid micropredation: the 20, 15, and 15 fish that were fed upon by gnathiids in each of the three gnathiid-exposed treatments died, whereas all fish that were exposed to but not fed upon by the gnathiids n( = 15, 18, and 15, respectively) survived (combined χ2 = 45.09, df = 2, P < 0.001; Table 2).

Discussion

Our field observations suggest that gnathiids in the Caribbean Sea can and will feed on a wide range of settlement-stage fish. These are the first such findings for the Caribbean region and one of only two studies to examine possible infestation by gnathiids of recently-settled coral reef fishes. Off Lizard Island, Great Barrier Reef, Sun et al. (2012) found high rates of parasitism at the time of settlement in Pomacentrus moloccensis Bleeker, 1853. However, they found no gnathiids and mini- mal prevalence of other reef-based parasites in larvae and post-settlement juveniles. In contrast, Grutter et al. (2011) found that about 3%–5% of small juveniles of this species collected at dawn at the same sites were infected with gnathiids, and Penfold et al. (2008) reported gnathiids from these sites in juvenile Acanthochromis polyacanthus (Bleeker, 1855) (which lack a pelagic larval stage) as small as 4.2 mm. The difficulty in detecting gnathiids on the most recently-settled reef fishes is likely attributable to the fact that gnathiid infestation is often fatal to them. In our field collections, we observed mortality associated with gnathiid infestation of the small- est settlement-stage fish. While we were unable to determine whether in these cases the gnathiids were the cause of death, a causal relationship was confirmed by our Artim et al.: Gnathiid micropredation on larval reef fish 485 laboratory experiments, where a single 3rd-stage gnathiid was sufficient to kill French grunt between 7 and 15 mm in length. Penfold et al. (2008) and Grutter et al. (2008) conducted similar laboratory studies using two damselfish species [A. polyacanthus and Neopomacentrus azysron (Bleeker, 1877)] from Lizard Island. In these studies, gnathiids were also directly linked to fish mortality. However, mortality rates were lower than in our study: fish <13 mm that were exposed to 1–3 gnathiids experienced mortality rates of up to 16%, while larger fish experienced no mortality. Even in the apparent non-lethal cases, the blood volumes withdrawn from the fish reported here are relatively large when compared with these fishes’ size and likely result in compromised host condition and performance. Because of the 100% mortality of fish fed upon by gnathiids in our experimental study, we did not examine sublethal effects. However, Grutter et al. (2011) reported that where small juvenile Pomacentrus amboinensis Bleeker, 1868 survived feeding by a single gnathiid, such fish consumed more oxygen, exhibited lower critical swimming speed, and had high- er mortality rates in the field compared with control fish. From an evolutionary perspective, our observations, combined with the studies cited above, are consistent with predictions of the hypothesis that escape from micropredators may be one advantage of a pelagic larval stage in reef fishes (Grutter et al. 2008, Sun et al. 2012). They further suggest that, while nocturnal settlement may enable recruiting reef fishes to avoid predation by diurnal piscivores, it could increase their exposure to nocturnal micropredators. Nocturnal micropredators and diurnal piscivores could therefore constitute opposing selective forces influencing when and where larval fish settle on reefs. Ecologically, the effect of gnathiids on recruitment, growth, and persistence of coral reef fishes will depend on encounter rates and on the susceptibility of individual fish to infestation once encountered. Encounter rates will be influenced by gnathiid density, which should depend on host availability, the abundance of gnathiid con- sumers, such as cleaners (e.g., Grutter 1996) and the benthic habitat in which gnathiids spend the majority of their time (e.g., Artim and Sikkel 2013). Gnathiid density at the site of our larval trapping study was approximately 150 gnathiids m−2 with the average greatest distance traveled by gnathiids in seeking a host-fish approximately 0.2–2.0 m (Artim and Sikkel, unpubl data). The chance of encounters between settlement stage fish and gnathiids would therefore seem high. Encounters between gnathiids and settlement-stage fish will be further mediated by host detectability, and the availability of alternative hosts combined with gnathiid host preferences. Gnathiids at our sites appear to use chemical cues to locate hosts at night (Sikkel et al. 2011) and certain hosts would be expected to produce stronger or more attractive cues. In general, smaller fish would seem to produce weaker cues and therefore be less likely to be detected, but may be easier to penetrate and feed upon once detected. At our study sites, susceptibility to gnathiids among adult-size fish varies both with body size and among species when body size is controlled for, with snappers and grunts being most susceptible (Coile and Sikkel 2013). The factors responsible for this variation remain unclear. However, it seems likely that similar differences would also occur among recently settled fishes. An understanding of body size–mortality relationships during early ontogeny and, thus, recruitment dynamics of fishes requires an understanding of all potential sources of early mortality (Pepin 2015). Given the demonstrated impact of even a single gnathiid, future studies should examine the multitude of factors that 486 Bulletin of Marine Science. Vol 91, No 4. 2015 influence gnathiid interaction with recently-settled fish and the conditions under which gnathiids and related micropredators contribute directly or indirectly to post- settlement and thus successful recruitment of coral reef fishes.

Acknowledgments

The authors gratefully acknowledge the field assistance and observations of E Brill, R Grippo, G Hendrick, A Hook, M Nicholson, T Rey Santos, S Robles, C Spitzer, and J Wagner. This work was funded in part by grants from the US National Science Foundation (OCE- 121615, and OCE-1536794, PC Sikkel, PI), and Puerto Rico Sea Grant (PC Sikkel, PI). This is contribution number 140 from the University of the Virgin Islands Center for Marine and Environmental Studies.

Literature Cited

Abràmoff MD, Magalhães PJ, Ram SJ. 2004. Image processing with ImageJ. Biophotonics Int. 11:36–43. Arnal C, Côté IM, Morand S. 2001. Why clean and be cleaned? The importance of client ectoparasites and mucus in a marine cleaning symbiosis. Behav Ecol Sociobiol. 51:1–7. http:// dx.doi.org/10.1007/s002650100407 Artim JM, Sikkel PC. 2013. Live coral repels a common reef-fish ectoparasite. Coral Reefs. 32:487–494. http://dx.doi.org/10.1007/s00338-012-0995-8 Bunkley-Williams L, Williams EH. 1998. Isopods associated with fishes: a synopsis and correc- tions. J Parasitol. 84:893–896. http://dx.doi.org/10.2307/3284615 Carr MH, Hixon MA. 1995. Predation effects on early post-settlement survivorship of coral- reef fishes. Mar Ecol Prog Ser. 124:31–42. http://dx.doi.org/10.3354/meps124031 Coile AM, Sikkel PC. 2013. An experimental field test of susceptibility to ectoparasitic gnathiid isopods among Caribbean reef fishes. Parasitology. 140:888–896. http://dx.doi.org/10.1017/ S0031182013000097 Farquharson C, Smit NJ, Sikkel PC. 2012. Gnathia marleyi sp. nov. (Crustacea, Isopoda, Gnathiidae) from the eastern Caribbean. Zootaxa. 3381:47–61. Ferreira ML, Smit NJ, Grutter AS, Davies AJ. 2009. A new species of gnathiid (Crustacea: Isopoda) parasitizing teleosts from Lizard Island, Great Barrier Reef, Australia. J Parasitol. 95:1066–1075. http://dx.doi.org/10.1645/GE-1920.1 Forrester GE, Steele MA. 2004. Predators, prey refuges, and the spatial scaling of density-dependent prey mortality. Ecology. 85:1332–1342. http://dx.doi.org/10.1890/03-0184 Grutter AS. 1994. Spatial and temporal variations of the ectoparasites of seven reef fish species from Lizard Island and Heron Island, Australia. Mar Ecol Prog Ser. 115:21–30. http:// dx.doi.org/10.3354/meps115021 Grutter AS. 1996. Parasite removal rates by the cleaner wrasse Labroides dimidiatus. Mar Ecol Prog Ser. 130:61–70. http://dx.doi.org/10.3354/meps130061 Grutter AS. 1999. Infestation dynamics of gnathiid isopod juveniles parasitic on the coral-reef fishHemigymnus melapterus (Labridae). Mar Biol. 135:545–552. http://dx.doi.org/10.1007/ s002270050655 Grutter AS, Pickering JL, McCallum H, McCormick MI. 2008. Impact of micropreda- tory gnathiid isopods on young coral reef fishes. Coral Reefs. 27:655–661. http://dx.doi. org/10.1007/s00338-008-0377-4 Grutter AS, Poulin R. 1998. Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Mar Ecol Prog Ser. 164:263–271. http://dx.doi.org/10.3354/meps164263 Artim et al.: Gnathiid micropredation on larval reef fish 487

Grutter AS, Crean AJ, Curtis LM, Kuris AM, Warner RR, McCormick MI. 2011. Indirect effects of an ectoparasite reduce successful establishment of a damselfish at settlement. Funct Ecol. 25:586–594. http://dx.doi.org/10.1111/j.1365-2435.2010.01798.x Hixon MA. 2015. Predation: piscivory and the ecology of coral-reef fishes. In: Mora C, editor. Ecology and conservation of fishes on coral reefs: the functioning of an ecosystem in a changing world. University of Hawai’i Press. p. 41–52. Jones CM, Grutter AS. 2005. Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol. 66:860–864. http:// dx.doi.org/10.1111/j.0022-1112.2005.00640.x Jones CM, Grutter AS. 2007. Variation in emergence of parasitic and predatory isopods among habitats at Lizard Island, Great Barrier Reef. Mar Biol. 150:919–927. http://dx.doi. org/10.1007/s00227-006-0416-z Jones CM, Grutter AS. 2008. Reef-based micropredators reduce the growth of post-settlement damselfish in captivity. Coral Reefs. 27:677–684. http://dx.doi.org/10.1007/ s00338-008-0383-6 Klitgaard AB. 1997. The distribution and habitats in the North Atlantic of two gnathiid species (Crustacea, Isopoda) and their reproductive biology in the Denmark Strait and north of Iceland. Medd Gronl Biosci. 47:1–32. Olson KR. 1992 Blood and extracellular fluid volume regulation: role of the reninangioten- sin system, kallikrein-kinin system, and atrial natriuretic peptides. In: Hoar WS, Randall DJ, Farrell AP, editors. Fish Physiology, Volume 12, Part B, The Cardiovascular System, Academic Press, San Diego. p. 135–254. Penfold R, Grutter AS, Kuris AM, McCormick M, Jones CM. 2008. Interactions between juvenile marine fish and gnathiid isopods: predation versus micropredation. Mar Ecol Prog Ser. 357:111–119. http://dx.doi.org/10.3354/meps07312 Pepin P. 2015. Death from near and far: alternate perspectives on size-dependent mortality in larval fish. ICES J Mar Sci. http://dx.doi.org/10.1093/icesjms/fsv160 Raffel TR, Martin LB, Rohr JR. 2008. Parasites as predators: unifying natural enemy ecology. Trends Ecol Evol. 23:610–618. http://dx.doi.org/10.1016/j.tree.2008.06.015 Schmidt-Nielsen K. 1997. Animal physiology: adaptation and environment. Cambridge University Press, London. p. 95. Sikkel PC, Schaumburg CS, Mathenia JK. 2006. Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish. Coral Reefs. 25:683–689. http://dx.doi.org/10.1007/ s00338-006-0154-1 Sikkel PC, Ziemba RE, Sears WT, Wheeler JC. 2009. Diel ontogenetic shift in parasitic activ- ity in a gnathiid isopod on Caribbean coral reefs. Coral Reefs. 28:489–495. http://dx.doi. org/10.1007/s00338-009-0474-z Sikkel PC, Sears WT, Weldon B, Tuttle BC. 2011. An experimental field test of host-finding mechanisms in a Caribbean gnathiid isopod and a new technique for sampling gnathiids on coral reefs. Mar Biol. 158:1075–1083. http://dx.doi.org/10.1007/s00227-011-1631-9 Smit NJ, Davies AJ. 2004. The curious life-style of the parasitic stages of gnathiid isopods. Adv Parasitol. 58:289–391. http://dx.doi.org/10.1016/S0065-308X(04)58005-3 Stobutzki IC, Bellwood DR. 1998. Nocturnal orientation to reefs by late pelagic stage coral reef fishes. Coral Reefs. 17:103–110. http://dx.doi.org/10.1007/s003380050103 Sun D, Blomberg SP, Cribb TH, McCormick MI, Grutter AS. 2012. The effects of parasites on early life stages of a damselfish. Coral Reefs. 31:1065–1075. http://dx.doi.org/10.1007/ s00338-012-0929-5 Tanaka K. 2007. Life history of gnathiid isopods—current knowledge and future directions. Plankt Benthos Res. 2:1–11. http://dx.doi.org/10.3800/pbr.2.1

B M S