Paul C. Sikkel

In situ evidence for ectoparasites as a proximate cause of cleaning interactions in reef fish

Although cleaning interactions are deemed a textbook example of mutualism, there is limited evidence that clients benefit from cleaning in terms of reduced ectoparasite loads. The proximate causes of cleaning behaviour are also contentious. We examined the effect of ectoparasite load (i.e. the number of larval gnathiid isopods) on client behaviour under natural conditions. Diel variation in gnathiid loads of longfin damselfish, Stegastes diencaeus, a common coral reef fish client of cleaning gobies (Elacatinus spp.), was correlated with variation in gnathiid emergence from the substratum at sites in both Puerto Rico and St John, northeastern Caribbean. Both benthic emergence of gnathiids and their infestation on damselfish peaked in the morning. Concomitantly, clients spent significantly more time posing for and being inspected by cleaners in the morning than at other times of day. Our results corroborate recent experimental results on captive clients and are consistent with the mutualistic interpretation of cleaning symbioses.

Diel infestation dynamics of gnathiid isopod larvae parasitic on Caribbean reef fish

Infestation dynamics of parasitic gnathiid isopods on Caribbean reefs were studied throughout the 24-h diel cycle. Gnathiid infestation on caged longfin damselfish (Stegastes diencaeus) peaked strongly at dawn, remained low during the remainder of the day, and increased again at night until about midnight. Gnathiids were less abundant during the pre-dawn period. Peak loads on fish retrieved at dawn were the highest reported in any study thus far. The dawn peak consisted almost exclusively of individuals from the smallest size class, whereas nocturnal activity consisted almost exclusively of individuals of the largest size class. Because of the high rates of infestation at night and dawn, and the high variation in parasite loads on fish collected during that time, reduction of parasite infestation may play an important role in the selection of nocturnal and crepuscular shelter holes and settlement sites by reef fishes.

Effects of three Caribbean cleaner shrimps on ectoparasitic monogeneans in a semi-natural environment

Most research on cleaning symbioses on coral reefs has focused on fish clients being cleaned by smaller fishes. While many shrimps and other crustaceans are reported as cleaners, whether they remove parasites from fish hosts and can effectively regulate populations of ectoparasites is unclear. The effects of Pederson shrimp (Periclimenes pedersoni), spotted shrimp (P. yucatanicus), and banded coral shrimp (Stenopus hispidus), on the parasitic monogenean Neobenedenia melleni on a host reef fish, blue tang (Acanthurus coeruleus), were investigated. The abundance and size of N. melleni from fish with and without access to shrimps in a semi-natural macrocosm was quantified. P. pedersoni had a strong effect on both the abundance and size of parasites. In contrast, P. yucatanicus and S. hispidus had no effect on the abundance of parasites but had a small yet statistically significant effect on average size. These data suggest that P. pedersoni can play a significant role in the biological regulation of at least some ectoparasites on Caribbean reef fishes, but further suggest that some other shrimps regarded as “cleaners” may have little or no effectiveness at removing parasites and underscore the need for further verification before this term is applied.

Low Susceptibility of Invasive Red Lionfish (Pterois volitans) to a Generalist Ectoparasite in Both Its Introduced and Native Ranges

Escape from parasites in their native range is one of many mechanisms that can contribute to the success of an invasive species. Gnathiid isopods are blood-feeding ectoparasites that infest a wide range of fish hosts, mostly in coral reef habitats. They are ecologically similar to terrestrial ticks, with the ability to transmit blood-borne parasites and cause damage or even death to heavily infected hosts. Therefore, being highly resistant or highly susceptible to gnathiids can have significant fitness consequences for reef-associated fishes. Indo-Pacific red lionfish (Pterois volitans) have invaded coastal habitats of the western tropical and subtropical Atlantic and Caribbean regions. We assessed the susceptibility of red lionfish to parasitic gnathiid isopods in both their native Pacific and introduced Atlantic ranges via experimental field studies during which lionfish and other, ecologically-similar reef fishes were caged and exposed to gnathiid infestation on shallow coral reefs. Lionfish in both ranges had very few gnathiids when compared with other species, suggesting that lionfish are not highly susceptible to infestation by generalist ectoparasitic gnathiids. While this pattern implies that release from gnathiid infestation is unlikely to contribute to the success of lionfish as invaders, it does suggest that in environments with high gnathiid densities, lionfish may have an advantage over species that are more susceptible to gnathiids. Also, because lionfish are not completely resistant to gnathiids, our results suggest that lionfish could possibly have transported blood parasites between their native Pacific and invaded Atlantic ranges.

HABITAT AND SPECIES DIFFERENCES IN PREVALENCE AND INTENSITY OF NEOBENEDENIA MELLENI (MONOGENEA: CAPSALIDAE) ON SYMPATRIC CARIBBEAN SURGEONFISHES (ACANTHURIDAE)

Abstract We quantified Neobenedenia melleni from the skin of Caribbean surgeonfishes (Acanthuridae) from June through October 2005 and 2007. Prevalence, or mean intensity of infection, or both, varied significantly among the 3 species, and among sites and between years for the most heavily infected species, blue tang (Acanthurus coeruleus). Among 6 sites sampled, no more than 12% of ocean surgeonfish (Acanthurus bahianus) were infected, compared with 10 to 100% of A. coeruleus. The prevalence of infection among doctorfish (Acanthurus chirurgus), collected at only 1 of the sites, was intermediate between the other 2 species (46%). Mean intensity (range) of infection for the few infected A. bahianus was 1 (1) to 3 (1–8), compared with 1.3 (1–2) to 14.3 (1–59) for A. coeruleus, and 2.5 (1–8) for A. chirurgus. Expected abundance of N. melleni on A. coeruleus from shallow bay sites was greater than for those from non-bay sites. Higher infections on A. coeruleus may be attributable to differences in habitat use, or susceptibility to infection, or both, compared to other species. Among site and between-year differences may be associated with differences in benthic habitat, or water conditions, or both. This system seems ideal for future comparative studies on the relationship between environmental variables and parasites on Caribbean coral reefs.

Enhanced understanding of ectoparasite: host trophic linkages on coral reefs through stable isotope analysis

Graphical Abstract

Parasite-mediated enemy release and low biotic resistance may facilitate invasion of Atlantic coral reefs by Pacific red lionfish (Pterois volitans)

Abstract Successful invasions are largely explained by some combination of enemy release, where the invader escapes its natural enemies from its native range, and low biotic resistance, where native species in the introduced range fail to control the invader. We examined the extent to which parasites may mediate both release and resistance in the introduction of Pacific red lionfish (Pterois volitans) to Atlantic coral reefs. We found that fewer lionfish were parasitized at two regions in their introduced Atlantic range (The Bahamas and the Cayman Islands) than at two regions in their native Pacific range (the Northern Marianas Islands and the Philippines). This pattern was largely driven by relatively high infection rates of lionfish by didymozoan fluke worms and parasitic copepods (which may be host-specific to Pterois lionfishes) in the Marianas and the Philippines, respectively. When compared with sympatric, native fishes in the Atlantic, invasive lionfish were at least 18 times less likely to host a parasite in The Bahamas and at least 40 times less likely to host a parasite in the Cayman Islands. We found no indication that lionfish introduced Pacific parasites into the Atlantic. In conjunction with demographic signs of enemy release such as increased density, fish size, and growth of invasive lionfish, it is possible that escape from parasites may have contributed to the success of lionfish. This is especially true if future studies reveal that such a loss of parasites has led to more energy available for lionfish growth, reproduction, and/or immunity.

PARASITISM IN PTEROIS VOLITANS (SCORPAENIDAE) FROM COASTAL WATERS OF PUERTO RICO, THE CAYMAN ISLANDS, AND THE BAHAMAS

Abstract:  Recently, Pterois volitans, a Pacific species of lionfish, invaded the Atlantic Ocean, likely via the aquarium trade. We examined for internal and external parasites 188 individuals from 8 municipalities of Puerto Rico collected during 2009–2012, 91 individuals from Little Cayman, Cayman Islands, collected during the summers of 2010 and 2011, and 47 individuals from Lee Stocking Island, Bahamas, collected during the summer of 2009. In total, 27 parasite taxa were found, including 3 previously reported species from lionfish, the digenean Lecithochirium floridense, the leech Trachelobdella lubrica, and an Excorallana sp. isopod. We also report another 24 previously unreported parasite taxa from lionfish, including digeneans, monogeneans, cestodes, nematodes, isopods, a copepod, and an acanthocephalan. Among these parasites, several were previously unreported at their respective geographic origins: We report 5 new locality records from Puerto Rico, 9 from Cayman Islands, 5 from the Bahamas, 5 from the Caribbean, and 3 from the subtropical western Atlantic region. Three parasites are reported to associate with a fish host for the first time. The parasite faunas of P. volitans among our 3 study sites were quite different; most of the species infecting lionfish were generalists and/or species that infect carnivorous fishes. Although our study did not assess the impact of parasites on the fitness of invasive lionfish, it provides an important early step. Our results provide valuable comparative data for future studies at these and other sites throughout the lionfish′s invaded range.

Variation in occurrence of the fish-parasitic cymothoid isopod, Anilocra haemuli, infecting French grunt (Haemulon flavolineatum) in the north-eastern Caribbean

Parasites constitute the majority of coral reef animal diversity and are believed to contribute significantly to host, community and trophic dynamics. Anilocra spp. are large conspicuous ectoparasitic isopods, making them ideal models for host–parasite studies. In the tropical western Atlantic and Caribbean, Anilocra haemuli infects the ecologically important French grunt (Haemulon flavolineatum). French grunt are trophic connectors between reef and seagrass environments, and how A. haemuli infection influences connectivity is unknown. As a first step in understanding the French grunt–A. haemuli association, we conducted reef surveys during three consecutive years to quantify the abundance and prevalence of infected fish on reef sites in the north-eastern Caribbean. We examined their correlations with fish population and aggregation size, and social affiliation. Annual infected fish abundance and prevalence per site ranged from 0–24 fish and 0–66%. Prevalence: (1) appeared autocorrelated within bays among years; (2) was inversely correlated with population and aggregation size, although the statistical significance varied; and (3) was greater for solitary than aggregating fish. Our study provides the most comprehensive dataset for prevalence of any Anilocra spp., and the necessary baseline data for future studies on Anilocra–host dynamics, and the effect of parasites on trophic and habitat connectivity.

Comparison of sampling methodologies and estimation of population parameters for a temporary fish ectoparasite

Characterizing spatio-temporal variation in the density of organisms in a community is a crucial part of ecological study. However, doing so for small, motile, cryptic species presents multiple challenges, especially where multiple life history stages are involved. Gnathiid isopods are ecologically important marine ectoparasites, micropredators that live in substrate for most of their lives, emerging only once during each juvenile stage to feed on fish blood. Many gnathiid species are nocturnal and most have distinct substrate preferences. Studies of gnathiid use of habitat, exploitation of hosts, and population dynamics have used various trap designs to estimate rates of gnathiid emergence, study sensory ecology, and identify host susceptibility. In the studies reported here, we compare and contrast the performance of emergence, fish-baited and light trap designs, outline the key features of these traps, and determine some life cycle parameters derived from trap counts for the Eastern Caribbean coral-reef gnathiid, Gnathia marleyi. We also used counts from large emergence traps and light traps to estimate additional life cycle parameters, emergence rates, and total gnathiid density on substrate, and to calibrate the light trap design to provide estimates of rate of emergence and total gnathiid density in habitat not amenable to emergence trap deployment.