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Carry-Over Effects Modulated by Salinity During the Early Ontogeny Of Comparative Biochemistry and Physiology, Part A 217 (2018) 55–62 Contents lists available at ScienceDirect Comparative Biochemistry and Physiology, Part A journal homepage: www.elsevier.com/locate/cbpa Carry-over effects modulated by salinity during the early ontogeny of the T euryhaline crab Hemigrapsus crenulatus from the Southeastern Pacific coast: Development time and carbon and energy content of offspring ⁎ Ángel Urzúaa,b, , Miguel Bascura,c, Fabián Guzmána,d, Mauricio Urbinae a Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile b Centro de Investigación en Biodiversidad y Ambientes Sustentables (CIBAS), Universidad Católica de la Santísima Concepción, Concepción, Chile c Programa de Magíster en Ecología Marina, Universidad Católica de la Santísima Concepción, Concepción, Chile d Programa de Magíster en Medio Ambiente, Universidad de Santiago de Chile, Santiago, Chile e Departamento de Zoología, Facultad de Ciencias Naturales y Oceanografía, Universidad de Concepción, Casilla 160-C, Concepción, Chile ARTICLE INFO ABSTRACT Keywords: Hemigrapsus crenulatus is a key species of coastal and estuarine ecosystems in the Southeastern Pacific and New Malacostraca Zealand. Since the gravid females-and their embryos-develop under conditions of variable salinity, we propose Salinity that low external salinity will be met with an increase in energy expenditures in order to maintain osmor- Reproduction egulation; subsequently, the use of energy reserves for reproduction will be affected. In this study, we investigate Life-cycle in H. crenulatus whether 1) the biomass and energy content of embryos is influenced by salinity experienced Cascade effect during oogenesis and embryogenesis and 2) how variation in the biomass and energy content of embryos affects Offspring condition Southeastern Pacific coast larval energetic condition at hatching. Here at low salinity (5 PSU), egg-bearing females experienced massive and frequent egg losses, and therefore the development of their eggs during embryogenesis was not completed. In turn, at intermediate and high salinity (15 and 30 PSU) embryogenesis was completed, egg development was successful, and larvae were obtained. Consistently, larvae hatched from eggs produced and incubated at high salinity (30 PSU) were larger, had higher dry weight, and had increased carbon content and energy than larvae hatched from eggs produced at intermediate salinity (15 PSU). From these results, it is seen that the size and biomass of early life stages of H. crenulatus can be affected by environmental salinity experienced during oo- genesis and embryogenesis, and this variation can then directly affect the energetic condition of offspring at birth. Therefore, this study reveals a “cascade effect” modulated by salinity during the early ontogeny. 1. Introduction Among marine invertebrates with complex life cycles are pleocye- mata decapods. These malacostracans incubate their eggs under their Benthic marine invertebrates with complex life cycles develop abdomens, and thus developing eggs experience the same environ- through different ontogenetic stages as eggs, planktonic larvae, and mental conditions as their mother (Pandian, 2016). In decapods, the benthic juvenile-adults (Calado and Leal, 2015; Jaeckle, 1995; Poulin newly laid eggs contain all of the energy reserves necessary for em- et al., 2001). Although each ontogenetic stage is distinctively different, bryonic development (Jaeckle, 1995). Therefore, initial biomass largely they are all closely linked to each other (Giménez, 2006; Podolsky and depends on these initial reserves and their subsequent use during em- Moran, 2006). For example, the effects of environmental conditions on bryogenesis (Anger, 2001). Despite this, egg development is also in- reproductive features of marine invertebrates can have important fluenced by environmental factors experienced during embryogenesis consequences on population size and structure (Allen and Marshall, such as temperature (Fischer et al., 2009; Wear, 1974), oxygen avail- 2010; Calado and Leal, 2015; Pechenik, 2006). In this context, the ability (Fernández et al., 2006), and salinity (Giménez and Anger, environmental conditions experienced during the embryonic phase 2001). Therefore, environmental conditions experienced before have been recognized as an important factor influencing larval per- hatching may also subsequently affect the performance and survival of formance, and therefore, indirectly affecting later benthic stages larvae (Calado et al., 2007; Guerao et al., 2012). (Giménez, 2010; Grosberg and Levitan, 1992). The maintenance of internal osmolality within tolerable levels is ⁎ Corresponding author at: Departamento de Ecología, Facultad de Ciencias, Universidad Católica Ssma. Concepción, Alonso de Ribera 2850, Concepción, Chile. E-mail address: [email protected] (Á. Urzúa). https://doi.org/10.1016/j.cbpa.2018.01.001 Received 2 November 2017; Received in revised form 3 January 2018; Accepted 3 January 2018 Available online 06 January 2018 1095-6433/ © 2018 Elsevier Inc. All rights reserved. Á. Urzúa et al. Comparative Biochemistry and Physiology, Part A 217 (2018) 55–62 crucial to life and is particularly important when organisms experience Lenga estuary (Díaz-Jaramillo et al., 2013; Moscoso et al., 2006), the conditions of variable salinity. Regardless of the strategy used (os- crabs were transferred to three experimental salinity treatments (5, 15 moregulation, osmoconformation, or a mixture of both), tolerating and 30 PSU). The experimental salinities were prepared by diluting changes in salinity is an energetically costly process that likely requires filtered seawater (30 PSU) with distilled water, and salinities were tradeoffs with other processes (Evans, 2008). Most marine animals measured with a Hanna Instrument model HI 98195 multiparameter maintain internal osmolality by pumping ions against a concentration sensor, calibrated daily following the manufacturer's instructions. To gradient (i.e. Na+-K+, ATPase). In fact, in brackish and estuarine wa- reach the final experimental salinity, daily changes of 5 PSU were ters salinity is one of the key factors affecting embryogenesis, en- carried out. Once reached the experimental salinity, crabs were accli- ergetics, and larval condition in marine animals in general (in- mated to one of three experimental salinity treatments for a month vertebrates: Rivera-Ingraham and Lignot, 2017; fishes: Urbina and (acclimatization period). Specifically, eight males and 16 females were Glover, 2015). In malacostraca for example, it has been described that randomly assigned to each of the experimental salinity treatments, and although female estuarine crabs select optimal microhabitats for em- each individual crab was placed in a mesh compartment (each com- bryonic development (Darnell et al., 2010; Forward et al., 2005; Spivak partment was 30 × 30 × 30 cm). Males and females of each salinity et al., 1994), the embryos mostly experience natural temporal varia- treatment were maintained in separate aquaria to avoid fecundation. bility and spatial heterogeneity in salinity that characterizes the ex- The abdomens (i.e. pleopods) of the females were checked daily for the ternal environment (Giménez, 2006; Ituarte et al., 2005). Therefore, in presence of eggs and thus to detect for the potential effect of pre-fer- estuarine crabs, the salinity experienced by embryos may affect not tilization before the mating experiments (see below) at different sali- only survival and energy partitioning during embryogenesis (Giménez nities. The animals were feed Mytilus chilensis ad libitum and were and Anger, 2001; Taylor and Seneviratna, 2005) but also larval en- maintained in individual 27 L aquaria with aerated water of the re- ergetic condition (i.e. measured as carbon and energy content) and spective salinity, a constant temperature of 13.5 ± 0.5 °C (i.e. average survival at hatching (Giménez and Torres, 2002; Torres et al., 2007). In water temperature in Lenga estuary during the study period, including fact, differences in egg size and early larval biomass have been found in the incubation time: Bascur, 2014), and a 12:12 h light:dark photo- highly variable estuarine conditions at both intra and inter population period. The water and the food in the aquaria were changed daily. levels (Boudour-Boucheker et al., 2016). Hemigrapsus crenulatus (Milne Edwards, 1837) (Decapoda, Var- 2.2. Mating experiments unidae) is a key invertebrate species of coastal and estuarine ecosys- tems in the Southeastern Pacific and in New Zealand (Retamal, 2000). After the acclimatization period (for details of conditions see Recent studies show that this decapod has efficient osmoregulatory and above), male and female crabs were randomly combined in 1:2 ratios in bioenergetic mechanisms to tolerate a wide range of environmental mesh compartments (each compartment was 60 × 60 × 60 cm) to fa- salinities (5–30 PSU) (Urbina et al., 2010; Urzúa and Urbina, 2017). cilitate mating and reproduction. Specifically, for each salinity treat- Since the gravid females and, subsequently, their embryos develop in ment there were eight replicates of one male with two females. The conditions of variable salinity in the estuaries that they inhabit mating groups were maintained at the same salinity, temperature, and (Grandjean, 1985; Urzúa and Urbina, 2017), we hypothesize that low feeding conditions utilized during the acclimatization period. Females external salinity will require
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