Active Parental Care, Reproductive Performance, and a Novel Egg Predator Affecting Reproductive Investment in the Caribbean Spiny Lobster Panulirus Argus J
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Clemson University TigerPrints Publications Biological Sciences 8-2016 Active parental care, reproductive performance, and a novel egg predator affecting reproductive investment in the Caribbean spiny lobster Panulirus argus J. Antonio Baeza Clemson University Lunden Simpson Clemson University Louis J. Ambrosio Clemson University Nathalia Mora Universidad del Valle Rodrigo Guéron Instituto Federal de Educação, Ciência e Tecnologia do Espírito Santo See next page for additional authors Follow this and additional works at: https://tigerprints.clemson.edu/bio_pubs Part of the Life Sciences Commons Recommended Citation Please use the publisher's recommended citation. https://bmczool.biomedcentral.com/articles/10.1186/s40850-016-0006-6 This Article is brought to you for free and open access by the Biological Sciences at TigerPrints. It has been accepted for inclusion in Publications by an authorized administrator of TigerPrints. For more information, please contact [email protected]. Authors J. Antonio Baeza, Lunden Simpson, Louis J. Ambrosio, Nathalia Mora, Rodrigo Guéron, and Michael J. Childress This article is available at TigerPrints: https://tigerprints.clemson.edu/bio_pubs/104 Baeza et al. BMC Zoology (2016) 1:6 DOI 10.1186/s40850-016-0006-6 BMC Zoology RESEARCH ARTICLE Open Access Active parental care, reproductive performance, and a novel egg predator affecting reproductive investment in the Caribbean spiny lobster Panulirus argus J. Antonio Baeza1,2,3*, Lunden Simpson1, Louis J. Ambrosio1, Nathalia Mora4,RodrigoGuéron5 and Michael J. Childress1 Abstract Background: We used the Caribbean spiny lobster Panulirus argus, one of the largest brooding invertebrates in the Western Atlantic, to test for the presence/absence of active parental care and to explore reproductive performance in large brooding marine organisms. Given [i] the compact and large embryo masses produced by P. argus, [ii] the expected disproportional increase in brooding costs with increasing embryo mass size, and [iii] the theoretical allometry of egg production with increasing body size, we predicted that parental females in this large species will engage in active brood care. We also predicted that larger broods from larger lobsters should suffer higher mortality and brood loss than smaller broods from smaller lobsters if parental care was minimal or absent. Lastly, we expected smaller females to allocate disproportionably more resources to egg production than larger females in the case of minimal parental care. Results: Females brooding early and late embryos were collected from different reefs in the Florida Keys Reef tract, transported to the laboratory, and maintained in separate aquaria to describe and quantify active parental care during day and night. A second set of females was retrieved from the field and their carapace length, fecundity, egg size, reproductive output and presence/absence of brood-dwelling pathogens was recorded. Laboratory experiments demonstrated that brooding females of P. argus engaged in active brood care. Females likely use some of the observed behaviors (e.g., abdominal flapping, pleopod beating) to provide oxygen to their brood mass. In Panulirus argus, females did not suffer brood loss during embryo development. Also, reproductive output increased more than proportionally with a unit increase in lobster body weight. Conclusions: Our results agree with the view that large brooding marine invertebrates can produce large embryo masses if they engage in active parental care and that the latter behavior greatly diminishes reproductive performance costs associated with producing large embryo masses. Lastly, we report on a nemertean worm that, we show, negatively impacts female reproductive performance. Background of embryos and/or larvae takes place (various bivalves The degree of parental care varies broadly among mar- and sea urchins [3, 4]). At another extreme, some ine invertebrates, even within monophyletic clades [1, 2]. species with abbreviated or direct development produce At one extreme, some groups do not provide any form large yolky eggs that are brooded and hatch as advanced of parental care, spawning small unfertilized or fertilized larval stages or juveniles. These early ontogenetic stages eggs into the pelagic environment in which development might remain in the parental brood chamber and/or dwelling for long periods of time and can be fed, * Correspondence: [email protected] 1 defended, and groomed by females (various seastars, iso- Department of Biological Sciences, 132 Long Hall, Clemson University, – Clemson, SC 29634, USA pods, and amphipods, among others [5 7]). In between 3Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad extremes, many species exhibit indirect development, Católica del Norte, Larrondo 1281, Coquimbo, Chile Full list of author information is available at the end of the article © 2016 The Author(s). Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Baeza et al. BMC Zoology (2016) 1:6 Page 2 of 15 and parental care is restricted to the protection of em- than the exception in brooding marine invertebrates still bryos incubated in bodily chambers of varying complex- remains an open question. ity (e.g., many crustaceans, including spiny lobsters [8]). In marine brooding invertebrates, brooding costs Explaining the evolution and adaptive value of parental should be considerable in large females from large spe- care is one of the most relevant yet still not completely cies, as they have the potential to produce massive em- understood problems in evolutionary biology [1, 2]. bryo masses and also suffer the putatively heavy costs of In marine brooding invertebrates, benefits to brooded brooding [31, 32]. Theoretical considerations suggest offspring include, but are not limited to, protection that the costs associated with brooding (i.e., oxygen against predators [5, 9, 10], protection from adverse abi- provision, grooming) increase non-linearly with in- otic conditions [5, 9, 10], and/or physiological provision- creases in brood mass, potentially resulting in the inabil- ing [11]. Still, brooding embryos in bodily chambers is ity of large adults to successfully rear all brooded not exempt of costs. For instance, reproductive perform- embryos [23–25]. Furthermore, with increases in body ance (i.e., fecundity, reproductive output) of parental fe- size, the capacity for egg production is also expected to males might decrease due to brood loss, in turn, driven scale at a pace greater than the space available for by increases in embryo volume during development, em- brooding, and thus, larger adults might be capable of bryo crowding and loss from the abdominal chamber producing more gametes than can be successfully [12]. Embryo masses accumulate sediment, detritus, bac- brooded [33, 34] (Fig. 1a). teria, algae, fungi, and many other epizootic organisms Overall, large species of brooding marine invertebrates (e.g., ciliates) that might further impact parental repro- should suffer exacerbated brooding costs, resulting in ductive performance [13–16]. Egg predators are known poor reproductive performance, unless these large par- to destroy embryo masses when experiencing population ental individuals allocate considerable time and energy outbreaks, impacting not only female fecundity but also to attending their broods [23]. Indeed, brood mass size the host population health [17–19]. Perhaps more im- and parental behaviors are likely interlinked; large paren- portantly, large densely packed embryo masses can be tal individuals with large broods either allocate a consid- considered living tissue but without a circulatory system erable amount of energy and time to brood their [20]. Most embryo masses are larger than the theoretical embryos, or suffer the costs in terms of reproductive 1 mm limiting thickness that allows sufficient oxygen performance, when producing large embryo masses. supply by diffusion [21] and oxygen limitation does Various studies during the last decades have demon- occur at their centers [20, 22, 23]. Oxygen depletion at strated that physiological costs (i.e., increased metabolic the interior of embryo masses has been shown to be rate) are considerable in females engaging in active par- severe, even early during embryo development, when ental care [20, 23, 35]. Yet, whether brooding costs also respiration rates of early embryos are much lower than result in diminished reproductive performance in large those of late embryos [20]. Hypoxic conditions do im- species of brooding marine invertebrates has been pact embryo development, often driving asynchronous poorly explored. Studies on large species are particularly development within embryo masses (e.g., periphery ver- relevant as it will help to test whether or not excessive sus center) [9, 24, 25] and even embryo mortality [26]. physiological costs associated to brooding large embryo Likely, parental behaviors exclusively directed toward masses limit the evolution of brooding