Effects of Cymatocarpus solearis (Trematoda: Brachycoeliidae) on its second intermediate host, the Caribbean spiny lobster Panulirus argus

PLOS ONE RESEARCH ARTICLE Effects of Cymatocarpus solearis (Trematoda: Brachycoeliidae) on its second intermediate host, the Caribbean spiny lobster Panulirus argus Tomás Franco-Bodek1, Cecilia Barradas-Ortiz2, Fernando Negrete-Soto2, Rossanna Rodrı́guez-Canul3, Enrique Lozano-Álvarez2, Patricia Briones-Fourzán ID2* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Posgrado en Ciencias del Mar y Limnologı́a, Universidad Nacional Autónoma de México, Ciudad Universitaria, Ciudad de México, Mexico, 2 Unidad Académica de Sistemas Arrecifales, Instituto de Ciencias del Mar y Limnologı́a, Universidad Nacional Autónoma de México, Puerto Morelos, Quintana Roo, Mexico, 3 Laboratorio de Inmunologı́a y Biologı́a Molecular, Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional-Unidad Mérida, Mérida, Yucatán, Mexico * Abstract OPEN ACCESS Citation: Franco-Bodek T, Barradas-Ortiz C, Negrete-Soto F, Rodrı́guez-Canul R, LozanoÁlvarez E, Briones-Fourzán P (2023) Effects of Cymatocarpus solearis (Trematoda: Brachycoeliidae) on its second intermediate host, the Caribbean spiny lobster Panulirus argus. PLoS ONE 18(9): e0287097. https://doi.org/10.1371/ journal.pone.0287097 Editor: Hudson Alves Pinto, Universidade Federal de Minas Gerais, BRAZIL Received: February 1, 2023 Accepted: May 29, 2023 Published: September 29, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0287097 Many digenean trematodes require three hosts to complete their life cycle. For Cymatocarpus solearis (Brachycoeliidae), the first intermediate host is unknown; the Caribbean spiny lobster Panulirus argus is a second intermediate host, and the loggerhead turtle Caretta caretta, a lobster predator, is the definitive host. Trophically-transmitted parasites may alter the behavior or general condition of intermediate hosts in ways that increase the hosts’ rates of consumption by definitive hosts. Here, we examined the effects of infection by C. solearis on P. argus by comparing several physiological and behavioral variables among uninfected lobsters (0 cysts) and lobsters with light (1–10 cysts), moderate (11–30 cysts), and heavy (>30 cysts) infections. Physiological variables were hepatosomatic index, growth rate, hemocyte count, concentration in hemolymph of cholesterol, protein, albumin, glucose, dopamine (DA) and serotonin (5-HT). Behavioral variables included seven components of the escape response (delay to escape, duration of swimming bout, distance traveled in a swimming bout, swim velocity, acceleration, force exerted, and work performed while swimming). There was no relationship between lobster size or sex and number of cysts. Significant differences among the four lobster groups occurred only in concentration of glucose (lower in heavily infected lobsters) and 5-HT (higher in heavily and moderately infected lobsters) in plasma. As changes in 5-HT concentration can modify the host’s activity patterns or choice of microhabitat, our results suggest that infection with C. solearis may alter the behavior of spiny lobsters, potentially increasing the likelihood of trophic transmission of the parasite to the definitive host. Copyright: © 2023 Franco-Bodek et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. PLOS ONE | https://doi.org/10.1371/journal.pone.0287097 September 29, 2023 1 / 19 PLOS ONE Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This study received funding from Universidad Nacional Autónoma de México (Program UNAM-DGAPA-PAPIIT, project IN206117 (https://dgapa.unam.mx/), granted to P. B.-F. The Consejo Nacional de Ciencia y Tecnologı́a (CONACYT-México) (https://conacyt.mx/) provided a Master’s scholarship (2018-000012-01NACF08432) for T.F.-B. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Effects of Cymatocarpus solearis on Panulirus argus Introduction Parasitism is an important factor influencing the composition and structure of populations and communities [1, 2]. Parasites can affect many phenotypical characteristics of their hosts, such as growth rate, reproductive rate, nutritional condition, fecundity, immune response, and concentration in the hemolymph of metabolites or neuromodulators, among others [3–5]. Alterations in neuromodulators may in turn cause behavioral changes that increase susceptibility of hosts to predation [4, 6–8]. Digenean trematodes (Platyhelminthes) are widely distributed parasites that usually require three hosts to complete their life cycle: a definitive host and two intermediate hosts [9]. Trematode eggs released in the definitive host’s feces are ingested by the first intermediate host, which is usually a gastropod [10]. Eventually, cercariae are produced in the body of the first intermediate host and released into the water. Upon finding a second intermediate host, the cercariae penetrate its body and migrate to the appropriate tissue, where they encyst, becoming metacercariae. Metacercariae infect the definitive host via consumption of the second intermediate host [10]. Trophically-transmitted parasites may alter the behavior, appearance, or general condition of intermediate hosts in ways that increase their rates of consumption by predatory definitive hosts (review in [6]) and, in some cases, the effects may be multidimensional [4, 7]. It is important to determine which traits of a host are affected by a parasite because, even if the effects are subtle, they could change the host population dynamics and, by extension, the communities where they live [11, 12]. Trophically-transmitted parasites tend to have more dire consequences for the intermediate hosts than for the definitive hosts because the intermediate host needs to be eaten for the parasite to complete its life cycle in a definitive host, where it attains sexual maturity and reproduces [13]. A wide variety of trematodes use crustaceans as second intermediate hosts [14, 15]. This is the case for Cymatocarpus solearis (Brachycoeliidae) [16]. Definitive hosts for C. solearis are marine turtles, particularly loggerhead turtles Caretta caretta [17, 18]. The first intermediate host for C. solearis has not been identified yet but, to date, three species of decapod crustaceans have been reported as second intermediate hosts: the hermit (...truncated)