Elsevier

Limnologica

Volume 79, November 2019, 125717
Limnologica

Food matters: Trophodynamics and the role of diet in the invasion success of Procambarus clarkii in an Atlantic Forest conservation area

https://doi.org/10.1016/j.limno.2019.125717Get rights and content

Abstract

Procambarus clarkii is an important invasive freshwater species whose ecological plasticity allows for its establishment in different kinds of environments; such plasticity is also reflected in its diet with two main consequences: invasion success and impact on native biota. In order to investigate P. clarkii’s feeding habits, examine how its diet varies both seasonally and among different demographic groups (reproductive males, non-reproductive males and females) and explore the two consequences mentioned above, we investigated the trophic role of this species in an Atlantic Forest conservation area in the city of São Paulo (Brazil). A total of 540 specimens collected monthly over a year were measured and weighed. Their stomachs were weighed and classified according to the degree of stomach fullness. Stomach contents were examined, and animal and plant matter weighed. Food items were identified to the lowest possible taxonomic level and the percentage of occurrence of each item was calculated, as well as the diet diversity. Collected data were compared according to seasons and demographic groups through the Analysis of Similarity and Similarity Percentage Analysis. The percentage of animal weight attributed to stomach weight and the degree of fullness of stomachs did not vary significantly among seasons; however, non-reproductive males had significantly less full stomachs. Diet composition was evenly balanced between plant and animal material for both reproductive males and females, while non-reproductive males consumed a lower proportion of animal matter. The diversity in diet composition was high in all seasons and for all demographic groups, although always slightly lower for non-reproductive males. The percentage of occurrence of food items evidenced high consumption of algae and macrophytes throughout the year. It also reflected the seasonal variation of consumed prey, with a shift in consumption of insects and microcrustaceans in spring and summer to decapods and amphibians in fall and winter. The dissimilarity in diet composition was more pronounced among demographic groups than among seasons, being non-reproductive males the most different, with higher ingesting of less evasive prey. Nonetheless, winter differed from other seasons and was the season with least different food composition among demographic groups, indicating a homogenization in diet composition, which might be due to restricted availability of resources. Procambarus clarkii at Jaraguá State Park demonstrated conspicuous dietary variability and flexibility. The occurrence of filled stomachs indicates that food resources are not a constriction for this population. The species presented a diversified and adaptable diet, foraging on algae and macrophytes, and preying on different vertebrate and invertebrate taxa. Its trophic plasticity favors successful establishment in invaded areas and summed to its notable voracity, P. clarkii offers a wide, variable and significant interaction in food webs, being able to generate major impacts on native species by its feeding habits.

Graphical abstract

The proportion of animal and plant matter seasonally consumed by Procambarus clarkii reproductive males (blue line), non-reproductive males (grey line) and females (red line) in Southeast Brazil and the main modifications on diet composition along the year. The oval shapes represent the stomach degree of fullness of reproductive males (blue), non-reproductive males (grey) and females (red) in each season.

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Introduction

The red swamp crayfish Procambarus clarkii Girard, 1852 is native to North America (Central Southern United States and Northeastern Mexico) and is an invasive species in four continents; this freshwater species is appreciated in culinary circles and in the pet trade (Gherardi et al., 2011; Loureiro et al., 2015a). Its economic importance is the main reason it has become widespread worldwide (Hobbs and Lodge, 2010; Hänfling et al., 2011). Many ecological characteristics contribute to its establishment success in distinct environments, ranging from its diverse feeding strategies to its capability of adjusting reproductive strategy, aggressiveness and burrowing behavior, according to environmental characteristics (Gutiérrez-Yurrita et al., 1999; Alcorlo et al., 2004; Gherardi, 2006; Loureiro et al., 2015a). Moreover, males of this species can alternate between two different morphotypes: 1- reproductive males (RM) that are distinguished by the presence of hooks on the ischia of the 3rd and 4th pereiopods and a more calcified copulatory organs (also referred as Type I Males); and 2- non-reproductive males (NRM) that are recognized by the absence of the aforementioned hooks (also referred as Type II Males) (Taketomi et al., 1990; Henttonen and Huner, 1999; Loureiro et al., 2015a). Males can alternate between morphotypes within their lifetime, even after reaching sexual maturity. This means an RM can become an NRM and then switch back to an RM (Taketomi et al., 1990).

Impacts associated to P. clarkii‘s establishment are diverse, but mostly related to predation, competition and transmission of diseases (Dorn and Wojdak, 2004; Rodríguez et al., 2005; Gherardi and Acquistapace, 2007; Longshaw, 2011). Focusing on predation consequences, feeding interactions may have ubiquitous effects on species richness, and ecosystem productivity and stability (Ricklefs, 2008). Indeed, crayfish species are known to induce profound changes in ecosystem organization and functioning, since they are considered key species that are able to control energy flow in invaded environments (Olsen et al., 1991; Momot, 1995; Souty-Grosset et al., 2016).

In addition to the association between foraging ecology and impact, diet is also related to invasion successes and severity (Zhang et al., 2010). The capability of crayfish to reach high densities is correlated to two main aspects: the great adjustability of their metabolic system by using energy from different food sources (animal and plant) (Musgrove, 1988) and the polytrophic feeding behavior that confers them a great feeding plasticity, by interchanging among detritivory, herbivory and carnivory (Momot, 1995). Procambarus clarkii is known to feed on plant and animal detritus, macrophytes and a variety of live animals such as molluscs, insects, annelids, nematodes, platyhelminthes, tadpoles, frogs, juvenile fish and other crustaceans (Gutiérrez-Yurrita et al., 1998a; Parkyn et al., 2001; Correia, 2002; Alcorlo et al., 2004; Cruz and Rebelo, 2005; Banci et al., 2013). Furthermore, understanding seasonal and intrapopulation variations of feeding strategies and identifying periods of food scarcity may allow population management through intensive population control during these periods. Identifying this period of higher susceptibility may improve the effects of population control as well as reduce investment of money and labor.

In Brazil, seventeen invasive locations are presently known, all in the state of São Paulo (Banci et al., 2013; Loureiro et al., 2015b), and few studies have accounted for the ecology and/or impacts of P. clarkii in Brazilian environments. Since this species presents great ecological plasticity and capability to change and adapt its ecological traits to different types of habitats (Alcorlo et al., 2004; Loureiro et al., 2015a), investigating P. clarkii’s feeding ecology in Brazil is of utmost importance to design specific management strategies. Hence, this study intends to complement studies from other locations regarding feeding ecology and diet of the red swamp crayfish in a natural habitat by investigating feeding behavior and seasonal variation, and relating these aspects to the potential harm posed by P. clarkii’s establishment. We also aim to identify whether or not a specific demographic group is under greater pressure and the period in which these animals are most vulnerable in order to suggest when population control efforts should be focused.

Section snippets

Study site and field work

Procambarus clarkii individuals were collected monthly, from December 2013 to November 2014, from a 1,058- m² natural eutrophic pond (1,058-m²), located in Jaraguá State Park (JSP), an Atlantic Forest conservation area in the state of São Paulo, Brazil (23°27′49.47″S - 46°45′17.86″ W) (Fig. 1). The park has an area of 4.93 km² and the average altitude is 900 m (range of 735 m – 1,125 m). The climate is CfB type (Temperate Oceanic Climate), according to Köppen’s classification (1948), with an

Morphometry

In total, 540 animals (180 RM, 180 NRM and 180 F) were measured, weighed, and had their stomach content analyzed. The mean POCL and TBWW were 30.72 mm and 14.86 g for RM, 23.50 mm and 13.06 g for NRM and 26.75 mm, and 14.59 g for F (Fig. 3A, B). Measurement data were normally distributed and with low skewness for RM (0.01) and NRM (0.06), but not for F (-0.47). The low frequency of large females captured in this study (right-skewed histogram) may be explained by their sheltering behavior during

Final remarks

Freshwater species distribution is shaped by the interactions among animal habits, habitat physical conditions and resources availability (including food) (Merritt and Cummins, 1984). For introduced species, this synergy of variables is also determinant, separating purely exotic species from those that really became invasive. When the recipient environment has available niche opportunities for introduced species, i.e. resources are not fully used, they have higher chances to become invaders.

Declaration of Competing Interest

None.

Acknowledgements

We are thankful to the National Council for Scientific and Technological Development of the Brazilian Government (CNPq) for a productivity fellowship granted to PBA. This research was also supported by the Coordination for the Perfecting of High Education Personnel (CAPES), the Graduate program in Animal Biology (UFRGS) and the Institute of Bioscience of the University of São Paulo (USP). We also thank COTEC-SP for fieldwork authorization and reviewers for comments and suggestions for the

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