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Unusual male size vs sperm count relationships in a coastal marine amphipod indicate reproductive impairment by unknown toxicants [1]
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Date: 2021-04-01
Healthy reproduction is a vital process to maintain the integrity of populations and ecosystems and gamete fertilization is a fundamental step to achieve successful reproduction. Spermatozoa are specialized cells used to transfer genetic information from males to eggs and their quality depends on a number of factors, like nutrition and other environmental conditions (Lewis and Ford, 2012). Sperm quality is essential for successful fertilization and has been measured by several metrics including sperm number, sperm viability, sperm motility, spermatophore size, acrosome reaction, melanization and spermatophore absence rate and energy content of spermatophores (Harlıoğlu et al., 2018). The most commonly used methods to determine sperm quality are sperm count, sperm viability and sperm motility (Harlıoğlu et al., 2018).
Sperm count and sperm concentration are the main parameters to assess sperm quality in mammals (Ravanos et al., 2018), insects (Strobl et al., 2019), and marine invertebrates (Harlıoğlu et al., 2018). Positive relationships between body size and sperm counts are already known in insects, with larger males having more sperm cells; however, these relationships may vary depending on the environment that the organisms live in (Strobl et al., 2019). In many crustaceans, larger males tend to produce significantly more quantities of sperm than smaller males (Rodríguez et al., 2007). This significant positive correlation between sperm counts and male weight was observed in many species (Peralta-Martínez et al., 2019; Rodríguez et al., 2007). It has been noted that larger amphipods have an advantage to pair with larger females in a process known as mate guarding (Elwood and Dick, 1990), so it is important to study whether this advantage is only because of the size or if sperm quality of larger males is also higher than sperm quality of smaller males. Positive correlations between adult male size and sperm counts have also been reported in amphipods, for example, in Echinogammarus marinus (Yang et al., 2008), Gammarus pulex (Galipaud et al., 2011) and Gammarus duebeni (Arundell et al., 2014). However, no relationship between these parameters were reported in G. duebeni (Dunn et al., 2006), G. pulex (Lemaître et al., 2009) and Gammarus roeseli (Couchoux et al., 2018). To date, no studies have looked carefully into the relationship between sperm counts and sperm viability with male size in the context of environmental pollution.
Sperm viability is related to the ability of sperm cells to survive and for enough time to reach the place of fertilization (Holman, 2009). It is usually measured with a combination of two fluorescent dyes, SYBR-14, which stains live cells in green, and propidium iodide, which stains dead cells in red, and the cells can be observed by flow cytometry or fluorescence microscopy (Lewis and Ford, 2012). This method is relatively quick, it has been used for more than 50 years in reproduction and fertility studies of human and domestic animals and only in the last decade it has been increasingly applied in ecological studies (Holman, 2009). Holman (2009) and Gress and Kelly (2011) recommended to always associate sperm viability with sperm count to avoid spurious results, since the sperm viability assay could kill cells and reduce viability. According to these authors, a non-linear positive correlation between sperm count and viability is usually associated with problems in the technique that kill sperm cells and in this case sperm count should be used as a covariate for the analysis. A positive relationship between sperm count and sperm viability was found in insect house cricket (Gress and Kelly, 2011).
Crustaceans, specifically amphipods, are ideal candidates as model organisms having been successfully used in ecotoxicology for decades due to their short life-cycles and capacity to be maintain and reproduce in the laboratory (Podlesińska and Dąbrowska, 2019). They are essential components of aquatic ecosystems because they occupy several trophic niches and serve as food for fish and birds (Glazier, 2014). Echinogammarus marinus is one of the most abundant amphipod species in coastal communities in the northeast Atlantic (Martins et al., 2014), and lives mainly associated with assemblages of macro algae Fucus spp. These amphipods have great importance in the structure and functioning of intertidal communities, as an active predator of other invertebrates and an important prey for wading birds (Martins et al., 2014). This species has been a potential model organism in many fields of study, like ecology (Maranhão et al., 2001), reproductive biology (Ford et al., 2003a) and ecotoxicology (Yang et al., 2008).
General observations in gammarid amphipods from temperate zones show that females typically produce several broods in succession in warmer months (Hyne, 2011). E. marinus population density usually have a clear seasonal variation, with peaks during summer months in Southern England (Guler, 2012), Portugal (Maranhão et al., 2001) and Southwest Netherlands (Vlasblom, 1969). Environmental parameters, specifically temperature, seems to impact reproductive process of the amphipods (Maranhão et al., 2001). Sexual activity and recruitment happen during all year in E. marinus population from Southern England (Guler, 2012) and Portugal; however, in Portugal the recruitment was minimum by the end of winter (Maranhão et al., 2001). There is limited information about the effects of contaminants on male amphipod reproduction (Lewis and Ford, 2012; Yang et al., 2008). Decreases in amphipod sperm counts have been observed following exposures to contaminants, like cyproterone acetate (Gismondi et al., 2017), methoxyfenozide, pyriproxyfen and cadmium (Trapp et al., 2014) in laboratory studies. In field studies in Scotland, amphipods collected from industrially polluted sites had been reported to have about 20 % significantly fewer sperm compared to the ones from reference sites (Yang et al., 2008). Studies assessing sperm viability have rarely been conducted in amphipods, although a reduction in viability of sperm cells has already been observed in amphipods exposed to ionizing radiation (Fuller et al., 2019). Low sperm counts and sperm viability in amphipods have been linked to fewer fertilized eggs and brood success (Dunn et al., 2006; Fuller et al., 2019), which highlights the potential impact that reduced sperm counts could cause at the population level. This has been modelled for different species of amphipods, indicating that a decrease in sperm counts below certain thresholds could lead to population level impacts (Ford et al., 2012).
The aim of this study was to compare sperm counts and animal weight, and sperm count and sperm viability relationships in E. marinus collected from England and Scotland using pre-published and previously unpublished field and laboratory data. Following an unusual observation that amphipods collected in one location (Langstone Harbour) in Southern England over a decade ago, had what appeared to be no or very little relationship between sperm count and weight, we compared datasets over a decade to determine the temporal significance of this finding. To complement this data we also recorded egg/embryo numbers from females from Langstone Harbour and compared to the published literature.
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