Anthropogenic activities have caused major changes on our planet through a process collectively named as climate change (IPCC, 2013), which is responsible for diverse impacts on aquatic organisms and ecosystems (Hays et al., 2005; Häder et al., 2011; Winder and Sommer, 2012). In coastal systems, these changes in climate affect the performance of individuals at various stages of their life history, influence the dispersal and recruitment at the population level and alter the abundance and the strength of interactions and trophic relationships (e.g., predator-prey) at the community level (Harley et al., 2006).

Coastal marine habitats, which play a key role from an ecological and a socio-economic point of view, seem to be very vulnerable to climate change (Cloern et al., 2014). Some of the most important effects of climate change on coastal systems include an overall decrease in the penetration of solar radiation due to increased runoff of dissolved and particulate material from terrestrial origin (Evans et al., 2006). In addition, increased amounts of nutrients, originated both from climate change (e.g., atmospheric deposition, wind, precipitation) and from increased land usage (e.g., agricultural and cattle activities) are introduced into estuaries and coastal areas (Findlay, 2005; Monteith et al., 2007). Still, organisms might be exposed to increased levels of solar ultraviolet radiation (280–400 nm) by at least two processes—the depletion of the ozone layer and/or the increased stratification of the water column due to global warming (Beardall et al., 2009; Häder et al., 2011).

UVR, either at normal or at increased levels cause a number of negative effects on aquatic organisms, among which some of the most documented effects are the reductions of productivity and growth rates in phytoplankton (Villafañe et al., 2003) and significant mortality, reduced fertility and changes in behavior in diverse zooplankton species and invertebrates (Tank et al., 2003; Przeslawski et al., 2005; Hansson and Hylander, 2009). Increased nutrient inputs are directly related to human activities, i.e., urban, industrial and agricultural effluents and urban pressure on the coast line (Figueroa and Korbee Peinado, 2010) and they occur mostly as in the form of nitrogen and phosphorus (Fong et al., 1998; Teichberg et al., 2010). The effects of such increments in nutrient availability are variable for estuarine organisms. Macroalgae, as well as benthic invertebrates, are highly affected by them and so these organisms can be used to evaluate the ecological status of coastal waters (Figueroa and Korbee Peinado, 2010).

The objective of the present study is to assess the potential impacts of UVR exposure and increase in nutrients input (i.e., via anthropogenic activity) on the amphipod Amphitoe valida (Smith, 1873) of the Chubut River estuary (Patagonia, Argentina). Because macroalgae can concentrate and bioaccumulate diverse chemical species dissolved in the water (including nutrients) carried by the river (Rabalais, 2002) we used algal specimens from two different rocky beaches, one close and one further away from the mouth of the river, to feed amphipods collected also from these two sites. We hypothesized that under a scenario of increased nutrients (e.g., from anthropogenic origin) the quality of the food consumed by amphipods will increase, and this would counteract the harmful effects of UVR on food consumption rate (FCR).

Preliminary studies conducted in the area (Valiñas, unpublished) revealed significant differences in the FCR between males and females of A. valida. Therefore, the results of our study are presented separately, by the sex of the amphipods. In addition, those previous studies also evidenced that macroalgae from BB and C had similar values of nitrogen and phosphorus, but differed in their carbon content, being higher in macroalgae from BB (8% more carbon content than in C). The same analysis on amphipod tissue revealed that males from BB had 11% more carbon content that males from C, while females from C had 9% more C than those from BB. Based on these differences, we decided to discriminate the FCR not only by sex, if also by beach on which the amphipods were collected.

Estuaries are considered important ecosystems from an ecological point of view because the exchange between the river and the sea allows for the settlement of populations adapted to a variable physico-chemical environment (Wilson, 2008). Moreover, these systems play a key role because they receive significant inputs of sediments, nutrients, and pollutants, which have important consequences for the organisms living there (Libes, 1992; Wetsteyn and Kromkamp, 1994) or in their proximity. In the case of the Chubut River, the input of nutrients is especially important due to human activities, e.g., through the use of fertilizers and input of effluents (Helbling et al., 1992). As a result, the area is characterized by a high productivity that supports an important fishery (Skewgar et al., 2007) as well as populations of birds and marine animals (Yorio and Quintana, 2008). In the last decades the Chubut River valley has increased its land use for agricultural purposes and herding, thus generating a large amount of nutrients via fertilizers that are carried out to the river. In addition, other pollutants by urban and industrial wastes are also transported into the estuary (Sastre et al., 1998; Commendatore and Esteves, 2004).

In estuaries and marine shore areas, mesoherbivores, like amphipods, constitute a high percentage of the macrofauna (Huang et al., 2006), playing an important role in the marine food web, as they are mainly responsible for the transfer of energy to higher trophic levels (Huang et al., 2006; Jacobucci and Pereira Leite, 2008). They also play an important role in controlling primary producers' biomass by grazing differentially on macrophytes, as they can select their preferred food (Ortega et al., 2010). Taking into account their importance for the upper (as food) and the lower (as macroalgal biomass control) trophic levels of the food web, any effect on the amphipod population could have serious consequences for the entire food web.

Our study indicates that there are significant interactions between the diets offered to the amphipods and the location from where the amphipods were collected (i.e., BB or C). For example, males from BB, tended to have higher FCR when fed on diets with high nutrient content (e.g., diets containing either BB₁₀ or C₁₀) than when fed on diets with low nutrient content (e.g., BB₁, C₁ or BB₁C₁ diets). In contrast, an inverse trend was observed in males from C, which showed higher FCR when fed on diets with low nutrient concentration as compared to those with high nutrient concentration.

Previous studies, conducted with different macroalgae species, have shown that increased nutrient concentrations improved the quality of the food and this changed the herbivory rate (Montgomery and Gerking, 1980; Hemmi and Jormalainen, 2002; Boyer et al., 2004). It is broadly accepted that, in general, higher quality foods enhance fitness and will be selectively consumed when available (reviewed by Stephens and Krebs, 1986; Cruz-Rivera and Hay, 2000). Thus, herbivores can optimize their diet by preferential consumption of macroalgae with a higher nutritional value (e.g., Barile et al., 2004; Ortega et al., 2010). However, some organisms can behaviorally compensate for the low quality of food by increasing their feeding rates (Rueda et al., 1991; Cruz-Rivera and Hay, 2001; Duarte et al., 2014). In doing so, herbivores may exhibit different behavioral strategies to fulfill their nutritional requirements. In our case, it is interesting to note that males from different beaches had different strategies with regard to their food consumption and optimization of the food resources. Males from C had higher FCR in low as compared to high nutrients, probably as a strategy to compensate the low quality of food, as it had been observed from other marine amphipods (e.g., Cruz-Rivera and Hay, 2000, 2001); but in the case of males from BB, no food compensation was observed. Compensation for low quality food has also been shown to be achieved by increasing food absorption efficiency (Simpson and Simpson, 1990), or by adjusting respiration rates (Graça et al., 1993). This latter was found in the amphipod Gammarus pulex, which could successfully compensate for low quality food by adjusting its respiration rate, rather than its ingestion rate. We cannot rule out the possibility that males from BB could have displayed some of these responses to compensate their requirements in low quality diets. The fact that males from BB tended to have higher FCR than males from C, when fed on diets with high nutrient content harvested from either location, could be related with differences in the physiology of organisms living in different places and adapted to different ambient conditions (i.e., different nutrient input in the intertidal area).

The changes in the FCR with different diets in the amphipod males seem to be related also to the responses of individuals to UVR, as the UVR inhibition of FCR was relatively high (49%) when fed with ambient nutrient diets, but the inhibition decreased significantly (9%) when males were fed on high nutrient concentration diets regardless from where the males were collected. Thus, our results lead to the conclusion that food quality significantly counteracts the deleterious effects of UVR on FCR of amphipod males. As we mentioned above, high quality food enhances fitness, as for example shown by Lastra et al. (2008) for the talitrid amphipod Megalorchestia corniculata that reached the highest growth rates when fed on high quality food. Also, Cruz-Rivera and Hay (2000) showed that Gammarus mucronatus grew larger and produced more gonads when feeding on high quality food. In spite of this, UVR may have important effects on aquatic communities by altering species composition and interactions, with consequences for community structure, food web processes, and ecosystem functions such as nutrient cycling (Bothwell et al., 1994; Rozema et al., 1997). In aquatic systems, the direct deleterious effects of UVR on invertebrate abundance (Bothwell et al., 1994; Kiffney et al., 1997; Tank et al., 2003) and survivorship (McNamara and Hill, 1999) have been well documented. However, most of the studies were performed with invertebrate zooplankton species and the knowledge about UVR effects on species composition and species interactions in the marine benthos is still scarce (but see Pavia et al., 1997; Vinebrooke and Leavitt, 1999). Even though we did not perform any measurement of A. valida fitness, our results indicate that amphipod fed with low quality food were in worse physiological conditions to cope with UVR than those fed on high quality food and were not affected by UVR. Similar deleterious effects of UVR on A. valida were observed in a previous study, where individuals fed on green macroalgae with low amount of mycosporine-like amino acids (MAAs). These organisms showed lower survival rates than those fed on a diet rich in these photoprotective compounds (Helbling et al., 2002).

On the other hand, an interesting result was that even though males from C showed food compensation in low quality diets, their FCR was indeed affected by UVR, in the same way as in males from BB; this suggests that food compensation for low quality food was not sufficient to counteract the UVR effects. As we mentioned before, the reduction of FCR by UVR when amphipods fed on ambient nutrient concentration can have direct effects on the individual fitness (i.e., growth, biomass production and reproduction). Taken into account the role that these mesoherbivores play in the trophic food web (Huang et al., 2006; Jacobucci and Pereira Leite, 2008), a detrimental effect in their fitness could have direct consequences on the entire food web. Thus, at least for FCR, eutrophication at the nutrient levels could have a positive effect on the population of males of A. valida, counteracting the effects of UVR.

Females also showed a significant interaction between the diets offered to the amphipods and the location from where the amphipods were collected, but the response was different from that for males. Females did not have such a clear distinction and had FCR values that were similar under high nutrient food, for individuals collected from either place. Only in the B₁C₁ diet females from BB tended to compensate the low food quality by increasing their FCR, but in general, it was not observed as a strategy to fulfill their nutritional requirements. As with males, possibly other mechanisms rather than compensation or consumption of high nutritional quality foods are involved in the scope of nutritional requirements. Unlike males, the effect of UVR was significant regardless of the location from where the amphipods as well as the food were collected, suggesting that the diets offered and the response to UVR were not related. Females reduced their FCR values under UVR regardless whether they fed on low or high quality food, which suggested that they are more vulnerable to radiation than males, as females could not reduce the effects of UVR when fed on high quality food. This result is of particular importance given that females are responsible for carrying the eggs and subsequently the newborns in their brood pouch and thus ensure the offspring in the population.

There is a high amount of evidence that herbivores can regulate vegetal populations by top-down control (i.e., invertebrates, Bortolus and Iribarne, 1999; fish, Burkepile and Hay, 2010). Based on our results on FCR, it seems reasonable to conclude that, in a scenario of eutrophication (as a result of anthropogenic activities) and high solar UVR levels, an increase in macroalgae food quality as a result of high nutrient inputs, could favor only males of A. valida, by reducing the negative effects of UVR on their FCR. Nevertheless, these nutrient inputs could lead to other problems that were not evaluated in this study. Under a high input of nutrients, macroalgae respond enhancing their growth and consequently their biomass (Pardal et al., 2000). If the level of nutrient input is highly elevated, the increment in biomass could be deleterious, producing hypoxia or anoxia as a result of oxygen depletion (Malone, 1987; Deegan, 2002; Diaz and Rosenberg, 2008), affecting the survival of organisms living on and near macroalgae (Diaz and Rosenberg, 2008), or causing migration, in the case of mobile organisms, to other parts of the intertidal (Pardal et al., 2000; Tyler and Targett, 2007). In a study performed in the eastern Atlantic Ocean (Pardal et al., 2000) it was observed that an increase in macroalgae biomass may favor A. valida populations, enhancing their growth production; however, extensive blooms, affecting the whole area of distribution of this species, had a strong negative impact and might result in their disappearance. Our work, presented here is one of the first evidences about how marine amphipods could respond to the interactive effects of UVR and increase in nutrients supply. Our original hypothesis was rejected in the case of females, while we could not reject it in the case of males. Further studies, focusing on organism fitness are needed to fully understand how these factors affected by anthropogenic activities, could modulate the population dynamics of this group that play a key role in the marine food web in intertidal environments.