Estuarine, Coastal and Shelf Science 139 (2014) 88e98

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Estuarine, Coastal and Shelf Science

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Exploring trophic strategies of exotic caprellids (Crustacea: ): Comparison between habitat types and native vs introduced distribution ranges

Macarena Ros a,b,*, José Manuel Tierno de Figueroa b,c, José Manuel Guerra-García a,b, Carlos Navarro-Barranco a,b, Mariana Baptista Lacerda d, Maite Vázquez-Luis e, Setuko Masunari d a Laboratorio de Biología Marina, Departamento de Zoología, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain b Jun Zoological Research Center, C/Los Jazmines n 15, 18213 Jun, Granada, Spain c Departamento de Zoología, Facultad de Ciencias, Universidad de Granada, Campus Fuentenueva, 18071 Granada, Spain d Departamento de Zoologia, Universidade Federal do Paraná, Caixa Postal 19023, Curitiba, Paraná, Brazil e Instituto Español de Oceanografía, Centre Oceanogràfic de les Balears, Moll de Ponent s/n, 07015 Palma de Mallorca, Spain article info abstract

Article history: The trophic ecology of non-native species is a key aspect to understand their invasion success and the Received 26 August 2013 community effects. Despite the important role of caprellid amphipods as trophic intermediates between Accepted 28 December 2013 primary producers and higher levels of marine food webs, there is very little information on their feeding Available online 8 January 2014 habits. This is the first comprehensive study on the trophic strategies of two co-occurring introduced caprellids in the Spanish coasts: Caprella scaura and Paracaprella pusilla. The diet of 446 specimens of Keywords: C. scaura and 230 of P. pusilla was analyzed to investigate whether there were differences in the feeding Paracaprella pusilla habits in relation to habitat characteristics (natural vs artificial hard substrata), type of host substrata Caprella scaura invasive species (bryozoans and hydroids) and native vs introduced distribution ranges (Brazil vs Spain). Results revealed diet analyses differences in diet preferences of the two species that have important implications for their trophic feeding habits behaviour and showed a limited food overlap, which may favour their coexistence in introduced areas. In gut content general terms, P. pusilla is a predator species, showing preference by crustacean prey in all of its life stages, while C. scaura feeds mainly on detritus. Although no sex-related diet shifts were observed in either of the species, evidence of ontogenetic variation in diet of C. scaura was found, with juveniles feeding on more amount of prey than adults. No diet differences were found between native and introduced populations within the same habitat type. However, P. pusilla exhibited a shift in its diet when different habitats were compared in the same distribution area, and C. scaura showed a flexible feeding behaviour between different host substrata in the same habitat type. This study shows that habitat characteristics at different scales can have greater influence on the feeding ecology of exotic species than different distribution ranges, and support the hypothesis that a switch between feeding strategies depending on habitat characteristics could favour invasion success. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction issue at a global scale (Zenetos et al., 2010) and a prominent object of study. Despite being a biogeographical phenomenon, most Biological invasions are one of the main conservation threats studies on invasive species have focused exclusively on their ecol- and have caused many species extinctions (Olden et al., 2004; ogy in the communities to which they have been introduced, and Simberloff, 2010). Accordingly, they have become an important have ignored the ecology of these species where they are native (Hierro et al., 2005). The trophic ecology of invasive species, which is necessary to understand the community-wide effects of in- vasions (Tillberg et al., 2007), has traditionally focused on the re- * Corresponding author. Laboratorio de Biología Marina, Departamento de Zoo- lationships between the trophic niche breadth and the invasion logía, Facultad de Biología, Universidad de Sevilla, Avda. Reina Mercedes 6, 41012 Sevilla, Spain. success or on the impact of the introduced species in the native E-mail address: [email protected] (M. Ros). community (Olden et al., 2004; Piscart et al., 2011). Thus, for

0272-7714/$ e see front matter Ó 2014 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecss.2013.12.033 M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98 89 example, it is accepted that omnivorous species or those with a substrata which they inhabit. Finally, taking into account that the broad trophic niche have more success than those with a special- introduced range of C. scaura is not only restricted to Spain, the last ized diet, and often that invasive species prey on or compete with aim (3) is to investigate the consistency of the diet preferences of autochthonous (indigenous) taxa (Barbosa and Castellanos, 2005; C. scaura associated with the same host substratum and under Simberloff, 2010). However, a few studies assess the trophic similar habitat characteristics in different regions of the Mediter- changes between native and introduced distribution ranges for a ranean Sea. particular species. For example, Tillberg et al. (2007) showed a shift in the diet of the ant invasive species after their establishment 2. Material and methods comparing its feeding habits between different distribution ranges. Amphipods are a very important group in the aquatic benthic 2.1. Study area communities (Jazdzewski, 1980) being a fundamental trophic link between primary producers and higher trophic levels (Woods, The field survey was conducted from May 2011 to November fi 2009). They also are very successful colonizers of arti cial hard 2012 in the native (south coast of Brazil) and in the introduced substratum, reaching high densities in harbours and marinas range (coastal localities of southern Iberian Peninsula and Balearic (Buschbaum and Gutow, 2005; Ashton et al., 2010) including Islands, Spain) of Caprella scaura and Paracaprella pusilla. In the case biofouling on ship hulls (Frey et al., 2009). Moreover, among crus- of C. scaura, additional coastal localities of central and southern taceans, their important role as invasive taxa has been indicated Italy, Corsica, Malta and Greece were sampled to investigate the (Zenetos et al., 2010), and an increased number of introduced homogeneity of the C. scaura diet in the introduced area. species belonging to this group have been recorded (Jazdzewski et al., 2002). Nevertheless, the invasive amphipod species, and 2.2. Sampling collection especially in marine environments, are still poorly studied (Zenetos et al., 2010). For freshwater species, a wider bibliography demon- In the introduced (Spain) and native range (Brazil), two habitats, strating their role as invasive is available (e.g. Grabowski et al., defined by hard substratum type (artificial vs natural), were selected 2007; Piscart et al., 2011). In general, most invasive crustaceans for comparison. Selection of sampling localities was based on the are omnivorous (Karatayev et al., 2009) and occasionally predators abundance of caprellid populations. As artificial habitats we (Hänfling et al., 2011). However, the trophic ecology of these species considered fouling communities associated to recreational marinas in their introduced range in comparison with their native range has while intertidal and subtidal rocky coastal shores (1e5 m deep) were been almost ignored. Exploring differences in the feeding habits of selected as natural habitats. In Brazil, both caprellid species were exotic species in relation to habitat characteristic in different dis- present in natural and artificial habitats while in Spain none of the tribution areas can help to understand the factors involved in the species were found in natural habitats. In each locality, the host invasion success by these species. substrata (bryozoans and hydroids) where the caprellid species were Caprella scaura Templeton, 1836 and Paracaprella pusilla Mayer, more abundant were collected directly by hand. Each substratum 1890 are the only two introduced caprellid amphipods in the was collected independently and all samples were fixed in situ in Mediterranean Sea. Although the origin area of both species is un- 90% ethanol. In the laboratory, caprellids were sorted and identified known, as occurs with most fouling species which inhabits harbours to species level. The studied species with the capture locations, host (Carlton, 1996), Brazil is included in the potential native range of the substrata and collection dates are given in Appendix 1. two species (Ros et al., 2013a, 2014). P. pusilla was described for the first time in Brazil and C. scaura, although it was described for the first time in Mauritius, was also recorded in Brazil only two years 2.3. Diet analyses later, in 1838. Both species are well established in Spanish coastal areas co-occurring in Cádiz (south Atlantic coast of Spain) and For the diet study, specimens were analyzed according to the Mallorca (Balearic Islands) (Ros et al., 2013a). However, P. pusilla has method proposed by Bello and Cabrera (1999) and previously used only been found in Spain, being considered a recent introduced in studies on Amphipoda gut content analyses (e.g. Guerra-García species in Europe, while C. scaura is widely distributed along the and Tierno de Figueroa, 2009; Navarro-Barranco et al., 2013; Váz- Mediterranean Sea and the southern Atlantic coast of the Iberian quez-Luis et al., 2013). Individuals were placed in vials with Hert- ’ w Peninsula, including Spain and Portugal, and it appears that it is wig s liquid and heated in an oven at 70 C for 6 h before ’ displacing other native caprellids such as Caprella equilibra (Guerra- mounting individuals on slides in Hertwig s liquid for study under García et al., 2011; Ros, unpubl. obs.). Although their current dis- microscope. We used a compound microscope equipped with an tribution is well studied, little is known about their feeding strate- ocular micrometre to estimate the percentage of absolute gut gies in their native and introduced distribution ranges. As the diet is content (at 40 as % total area occupied by the contents in the the product of a feeding strategy (Kleppel, 1993), one may gain whole digestive tract) and the relative abundances of food items in insight into the ways in which caprellid species respond to their the gut content (at 400 as % area occupied by each component of food environments by measuring their diets. The only data on the the total gut contents). feeding habits of C. scaura and P. pusilla, based on its diet, were re- ported by Guerra-García and Tierno de Figueroa (2009) from a few 2.4. Statistical analyses individuals in a general study of the caprellid diet. Moreover, it re- mains unclear whether these two species differ in dietary prefer- To explore global differences among the diet of sex/age groups ences or if they are able to shift their feeding pattern according to for each species (considering as variable the percentage of the the habitat characteristics or with the sex and the development dominant food items), one way ANOVA was used. To test possible stage. diet differences for each species between native and introduced The aims of the present study are: (1) to describe in detail the ranges in different substrata associated with artificial habitats, a diet of Caprella scaura and Paracaprella pusilla according to the two-way ANOVA was used with the following factors: ‘distribution different sex/age groups, and (2) to analyze the differences in the range’,afixed factor with two levels: native and introduced; feeding pattern of both species in relation with native and intro- ‘substratum’,afixed factor and orthogonal, with two levels: the duced ranges, natural and artificial habitats and different host hydroid Eudendrium sp. and the bryozoan Bugula neritina for 90 M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98

Paracaprella pusilla, and the bryozoans B. neritina and Zoobotryon between substrata in both distribution ranges for Caprella scaura; verticillatum for Caprella scaura. the percentage of detritus in their gut was higher in Zoobotryon Taking into account that none of the species has been found in verticillatum (100 0, mean standard error) than in Bugula natural habitats in their introduced range, to test possible differ- neritina (93.4 1.2) (Su, p < 0.05; Fig. 2, Table 3). In the native ences in the diet of each species between artificial and natural range, when the influence of the habitat (artificial vs natural) was habitats, only the native range was considered (Brazil). For Caprella tested, we found significant differences for Paracaprella pusilla scaura, a two-way ANOVA was used with the following factors: (Fig. 3; Table 4), with higher percentages of prey in the artificial ‘habitat’,afixed factor with two levels: artificial and natural; and (87.6 3.7) than in natural habitat (60.0 9.9) (Fig. 4). These dif- ‘substratum’,afixed factor and orthogonal, with two levels: the ferences were also observed by MDS analysis in which P. pusilla bryozoans Bugula neritina and Zoobotryon verticillatum.ForPara- collected from artificial habitat are clearly separated from the caprella pusilla only one substratum was available for comparison in specimens collected from natural one (Fig. 5). This analysis also both habitats (Eudendrium sp.). Consequently, to test differences showed a limited food overlap based on a clear difference between among habitats for this species, one-way ANOVA was used. the diets of the two exotic species. The total number of specimens available with detected digestive contents differed among samples. Therefore, to properly conduct 4. Discussion balanced ANOVA designs, we always chose the lesser sample size for each treatment and we selected randomly the same number of 4.1. Feeding strategies of Caprella scaura and Paracaprella pusilla specimens from each sample. Prior to ANOVA, heterogeneity of variance was tested with Cochran’s C-test. Data were transformed In general, Caprella scaura is mainly a detritivorous species while with the Ln (x þ 1) if variances were significantly different at Paracaprella pusilla is a carnivorous one, based on the dominant p < 0.05. Where variances remained heterogeneous, untrans- food item found in the gut content of all of the sex/age categories formed data were analyzed, as ANOVA is a robust statistical test and considered. However, both species feed on a high variety of items is relatively unaffected by heterogeneity of variances, particularly being able to display different feeding strategies. Although no sex- in balanced experiments (Underwood, 1997). In such cases, to related diet shifts were observed in either of the species, an age- reduce type I error, the level of significance was reduced to <0.01. related diet shift was observed in C. scaura, where juveniles pre- Univariate analyses were conducted with GMAV5 (Underwood sented higher amount of prey and lower amount of detritus than et al., 2002). The affinities among species populations according the rest of sex/age groups considered. A diet shift during the to the dietary analysis were explored by MDS analysis using development has also been observed in other amphipods such as UPGMA and BrayeCurtis similarity index. Data of the area occupied Talitrus saltator (Olabarría et al., 2009) and has been reported as an for each component within the total gut content were considered important factor contributing to variation in diet within species (Guerra-García and Tierno de Figueroa, 2009). The multivariate (Hoeinghaus and Davis, 2007). Ontogenetic shifts in diet may occur analysis was carried out using the PRIMER v.5 package (Clarke and in order to overcome physiological constraints (Hentschel, 1998; Gorley, 2001). Rossi et al., 2004). For instance, when juveniles have physiolog- ical limitation in the maximum rate of food uptake, they might rely 3. Results on higher quality sources of food to minimize the amount of food and maximize energy uptake (Hentschel, 1998). This could explain We examined 446 specimens of Caprella scaura and 230 of the observation that juveniles of C. scaura collected from Bugula Paracaprella pusilla. From these, digestive contents were found in neritina presented a higher percentage of prey items than juveniles 419 specimens of C. scaura (Tables 1 and 2) and 168 of P. pusilla of C. scaura collected from Zoobotryon verticillatum, since the last (Table 1). Gut contents of the two studied exotic species included substratum retained more sediment than the former one (Ros et al., detritus, prey (crustaceans, and hydroids), macroalgae, 2013b), providing an advantage to take detritus. microalgae (e.g. diatoms) and dinoflagellates. The dominant In addition, a biogeographical perspective is needed to establish component in C. scaura was detritus in all the sex/age groups, while the degree of specificity in the feeding strategy at different habitats crustacea (mainly harpacticoid ) were the dominant item and distribution ranges. In the case of Paracaprella pusilla, although in P. pusilla (Fig. 1). There were no significant differences in the diet we did not observe differences in its trophic habits between its of the different sex/age groups for both species, except for the ju- native and introduced distribution ranges, we observed a clear veniles of C. scaura, which showed lower values of detritus (F ¼ 4.7, difference in the feeding strategy of this species when the diet of p < 0.01) and higher values of prey (F ¼ 6.6, p < 0.01) than the populations from artificial and natural habitats was compared. In remaining sex/age categories. The analysis of the gut contents of the artificial habitat, P. pusilla fed mainly on crustacean prey, pre- C. scaura in different localities of the Mediterranean Sea also dominantly harpacticoid copepods (more than 80% of its gut con- showed that the diet was also clearly dominated by detritus, apart tent). In natural habitats prey represented only the 60% of its gut from the case of Malta where the percentage of crustaceans content, with a considerable amount of detritus. This could repre- reached 45% (Table 2). This suggests that C. scaura is a primary sent a potential adaptation to food resources. Detritus feeding may detritivorous species, while P. pusilla is a primary carnivorous be important for carnivores when temporarily there is no available taxon, with more than 50% of prey in the gut content. In C. scaura, prey (Mayer et al., 2008), thus, the pycnogonid Ammothella longipes the average area occupied by the content in the whole digestive appears to be a carnivore during spring and early summer but tract ranged from 46.1% to 81.9% in Bugula neritina and from 52.5% seems to feed on detritus when availability of prey diminishes to 81.6% in Zoobotryon verticillatum.InP. pusilla, mean values during winter (Soler-Membrives et al., 2011). With regard to Cap- ranged from 22.0% to 38.2% in B. neritina and 33.2e54.2% in rella scaura, the consistency of gut content found across different Eudendrium sp. habitats, host substratum and distribution ranges suggests that When the influence of distribution range (native vs introduced) detritus is a food type that remains available in the different hab- in the dietary composition was evaluated, no significant differences itats studied. Vázquez-Luis et al. (2013) studied the influence of the were found for any of the studied species within the same habitat habitat type in the feeding habits on amphipods associated to characteristics (artificial habitats) (Table 3). However, the per- macroalgae and found that detritivore species showed the least centage of the main food items showed significant differences differences with respect to changes in habitats and substrata in M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98 91

Table 1 Gut contents of C. scaura and P. pusilla in different ranges (introduced and native), habitats (artificial and natural) and substrata (Bug: Bugula neritina; Zoo: Zoobotryon ver- ticillatum; Eud: Eudendrium sp.). M: males, Fm: mature females (with developed oostegites), Fp: premature females (with undeveloped oostegites), J: juveniles, T: total. N: number of specimens of each category examined, n: number of specimens with detected digestive contents. % Abs: total area occupied by the content in the whole digestive tract. Det: detritus, Cru: crustaceans, Pol: polychaetes, Hyd: hydroids, MAlg: Macroalgae; malg: microalgae, Din: dinoflagellates. Total values are indicated in bold.

Caprellid Range/habitat Substrate Sex/age N/n Components (100%) species group %Abs %Det %Cru %Pol %Hyd %MAlg %malg %Din

Caprella Introduced/artificial Bug M 33/32 81.1(3.9) 98.1(1.0) 1.6(1.0) e 0.3(0.3) eee scaura Fm 15/15 88.3(2.7) 99.3(0.7) 0.7(0.7) ee e ee Fp 7/7 87.1(4.7) 95.7(3.0) 4.3(3.0) ee e ee J 64/61 80.2(2.3) 92.0(2.0) 4.3(1.3) e 3.0(1.4) ee0.7(0.2) T 119/115 81.9(1.7) 94.9(1.2) 3.1(0.8) e 1.7(0.8) ee0.3(0.1) Zoo M 38/36 81.4(3.6) 100.0(0.0) eeeeee Fm 8/7 85.7(3.7) 100.0(0.0) eeeeee Fp 9/9 89.9(2.6) 100.0(0.0) eeeeee J 50/49 79.9(3.0) 100.0(0.0) eeeeee T 105/101 81.6(2.0) 100.0(0.0) eeeeee Native/artificial Bug M 17/17 73.5(5.4) 90.6(3.9) 1.5(1.2) 4.1(3.5) 2.4(1.3) 1.5(1.2) ee Fm 3/3 70.0(0.0) 93.3(6.7) 6.7(6.7) ee e ee Fp 16/16 60.6(4.7) 94.4(2.5) 1.9(1.9) e 0.3(0.3) 2.2(1.4) 1.3(0.7) e J 10/10 77.0(2.1) 91.5(2.2) e 2.0(2.0) 3.5(1.5) 2.5(1.3) 0.5(0.5) e T 46/46 69.6(2.7) 92.3(1.8) 1.6(0.9) 2.0(1.4) 1.7(0.6) 1.8(0.7) 0.5(0.3) e Zoo M 26/25 70.8(3.3) 100.0(0.0) eeeeee Fm 12/12 69.2(3.4) 100.0(0.0) eeeeee Fp 9/8 71.3(3.5) 100.0(0.0) eeeeee J 2/2 45.0(15.0) 100.0(0.0) eeeeee T 49/47 69.4(2.2) 100.0(0.0) eeeeee Native/natural Bug M 7/5 58.8(10.2) 97.0(1.2) eeee3.0(1.2) e Fm 2/1 20.0(e) 100.0(e) eeeeee Fp 2/2 45.0(5.0) 9.5(2.5) eee 2.5(2.5) 5.0(5.0) e J 1/1 15.0(e) 95.0(e) eee 5.0(-) e T 12/9 46.1(7.9) 96.1(1.1) eee 0.6(0.6) 3.3(1.2) e Zoo M 2/2 65.0(15.0) 100.0(0.0) eeeeee Fm 5/3 46.7(17.6) 86.7(13.3) 3.3(3.3) ee 10.0(10.0) ee Fp 4/3 50.0(15.3) 100.0(0.0) eeeeee J 0/0 eeeeeeee T 11/8 52.5(8.6) 95.0(5.0) 1.3(1.3) ee 3.8(3.8) ee Paracaprella Introduced/artificial Bug M 13/7 26.4(12.0) 21.4(9.3) 77.9(9.1) e 0.7(0.7) eee pusilla Fm 9/3 26.7(12.2) 30.0(21.1) 70.0(21.1) ee e ee Fp 14/7 15.7(3.0) 30.0(12.6) 70.0(12.2) ee e ee J 9/5 22.0(6.1) 4.0(3.3) 96.0(3.3) ee e ee T 45/22 22.0(4.4) 21.4(5.7) 78.4(5.7) e 0.2(0.2) eee Eud M 20/17 53.2(5.6) 19.1(6.8) 75.3(7.4) e 5.0(3.1) 0.6(0.6) ee Fm 16/11 56.4(6.8) 17.7(7.7) 82.3(7.7) ee e ee Fp 7/6 50.0(6.3) 16.7(7.3) 74.2(8.2) e 8.3(6.6) ee0.8(0.8) J 3/3 60.0(11.5) 30.0(30.0) 51.7(24.6) e 16.7(16.7) ee1.7(1.7) T 46/37 54.2(3.5) 19.2(4.5) 75.3(4.7) e 5.0(2.2) ee1.1(0.4) Native/artificial Bug M 24/18 48.3(5.5) 12.8(5.6) 86.9(5.6) ee e 0.3(0.3) e Fm 27/20 32.2(4.4) 6.0(3.3) 91.5(5.3) e 2.5(2.4) eee Fp 7/7 30.0(30.3) 31.4(9.12) 65.7(8.4) ee e 1.4(1.4) 2.8(2.8) J 4/3 36.7(8.8) 16.7(16.7) 83.3(16.7) ee e ee T 62/48 38.2(3.1) 12.9(3.2) 85.5(3.6) e 1.0(1.0) e 0.3(0.2) 0.4(0.4) Eud M 33/29 49.0(4.4) 25.3(5.7) 74.1(5.6) ee 0.2(0.2) 0.3(0.2) e Fm 9/7 47.8(4.7) 22.9(9.8) 76.4(9.6) ee e 0.7(0.7) e Fp 5/4 67.5(8.7) 37.5(3.7) 62.5(3.8) ee e ee J 5/3 43.3(6.7) 43.3(29.7) 56.7(29.6) ee e ee T 52/43 50.1(3.3) 27.3(4.6) 72.2(4.5) ee 0.1(0.1) 0.4(0.2) e Native/natural Eud M 16/7 22.1(7.1) 57.1(15.3) 36.5(16.1) 0.7(0.7) e 5.7(3.0) e Fm 17/10 42.2(6.2) 26.7(10.9) 58.3(10.3) 15.0(5.4) eee Fp 1/0 eeeeeeee J 1/1 30.0() 100.0() eeeeee T 25/18 33.2(4.9) 37.7(9.3) 51.8(9.2) e 8.2(3.3) e 2.3(1.3) e which they inhabit. In our study, we observed a change in the populations of C. scaura studied, including those that are invading proportion of detritus in the gut content of C. scaura when pop- different countries of the Mediterranean. Only in the case of the ulations inhabiting different substrata were compared; particularly population of Malta, a high percentage of prey in its gut content populations associated with Zoobotryon verticillatum fed practically (45%) was observed, reflecting that the species exhibits a plasticity only on detritus while populations associated with Bugula neritina feeding behaviour in its introduced range and possibly can adapt its fed also on other items but in low proportion. These small but diet regarding to the proportion of food items available. significant differences could be related to the spatial structure of B. neritina, which host a high diversity of epiphytic fauna (Conradi, 4.2. Feeding ecology and invasion success 1995), and may favour the occasional ingestion of small crustaceans or polychaetes by C. scaura, especially in the case of juveniles of this The different trophic strategies observed in the two caprellid species. Despite this, detritus was the dominant item in all species may have important consequences in their invasion success 92 M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98

Caprella scaura at various level of the invasion process. Caprella scaura is mainly a fi 100% lter-feeder and a scraping species in all habitat types and distri- bution range studied, but occasionally it can display predator and herbivore behaviour, since we found prey (including polychaetes, hydroids and crustaceans) and macroalgae in its gut content. Based 80% on the same factor, Paracaprella pusilla is also able to alternate between a predatory mode in artificial habitats and a combination between predatory and filter-feeding/scraping behaviour in natural ones. This agrees with Caine (1978) who observed that ambush 60% was the most frequently used strategy for obtaining food by this genus, although it commonly utilized other feeding modes. In contrast, Guerra-García and Tierno de Figueroa (2009) found that 40% P. pusilla fed exclusively on detritus based on the gut content of few specimens which presented a low proportion of absolute gut con- tent. This low proportion is common in carnivorous amphipod species and sometimes makes the analyses of their diet difficult 20% (Guerra-García et al., 2014). With respect to prey sizes, both species are able to use macro- and microphagous feeding modes to consume food items ranging in size from small crustaceans to fine

0% particles of detritus. This implies a high plasticity in their feeding Males Mature Premature Juveniles strategies and high ability to assimilate a wide spectrum of foods, females females which must contribute to the ability of both species to persist and colonize new and variable habitats. Caprella mutica, a successful exotic caprellid in the northern hemisphere, is fundamentally a Paracaprella pusilla detritivorous species (Guerra-García and Tierno de Figueroa, 2009), 100% but Cook et al. (2010) suggested that its flexible feeding strategy play an important role in its invasion success. The trophic niches of Paracaprella pusilla and Caprella scaura are

80% segregated in their introduced range, since P. pusilla prefers to feed on crustaceans while C. scaura feeds mainly on detritus. This could avoid an interspecific competition for the same food item and possibly favours the coexistence of both species in the same 60% introduced areas and even the same substratum types. This coex- istence was pointed out by Ros et al. (2013b) in the substratum Eudendrium racemosum in southern Spain. Ship fouling and ballast water have been suggested as the most 40% probable dispersal vectors for Paracaprella pusilla (Mead et al., 2011; Ros and Guerra-García, 2012). Taking into account that the main crustacean prey observed in its gut content were small har- 20% pacticoid copepods, and that copepods are the most abundant metazoan in ballast waters (Smith et al., 1999), this feeding habit could facilitate the dispersal of this species by these means. Pre- dation is also an important part of food acquisition in the invasive 0% amphipod Dikerogammarus villosus (Sowinsky, 1894), a very suc- Males Mature Premature Juveniles cessful invader of freshwater ecosystems in Europe. Once in the females females introduced range, P. pusilla would need to be established in artificial habitats such as harbours or artificial marinas. The eutrophication Detritus Crustaceans Hydroids Others that characterize these habitats due to anthropogenic activities may cause the replacement of large copepods with small ones (Uye, Fig. 1. Global mean percentage of each food item for the different sex/age groups for 1994). This could favour the increase of small harpacticoid the studied caprellid species. populations (the preferred diet item for P. pusilla) in the recipient habitat.

Table 2 Gut contents of Caprella scaura associated to Bugula neritina in different localities of the Mediterranean. N: number of specimens of each category examined, n: number of specimens with detected digestive contents. % Abs: total area occupied by the content in the whole digestive tract. Det: detritus, Cru: crustaceans, Pol: polychaetes, Hyd: hydroids, MAlg: Macroalgae; malg: microalgae, Din: dinoflagellates.

N/n %Abs Components (100%)

%Det %Cru %Pol %Hyd %MAlg %malg %Din

Greece 19/18 56.7(6.1) 82.2(6.7) 17.2(6.8) ee 0.6(0.4) ee Civitavechia 20/19 40.0(4.7) 98.4(1.6) 1.6(1.6) ee e e e Malta 23/21 58.8(4.5) 50.7(5.7) 45.0(6.4) ee 1.9(1.5) 2.4(0.9) e Palermo 22/20 63.0(5.0) 88.5(4.8) 11.5(4.8) ee e e e Ajaccio 20/15 49.3(8.2) 66.7(8.1) 18.0(8.1) ee 4.0(1.6) e 1.3(0.9) M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98 93

Fig. 2. Diet preferences of Caprella scaura based on the percentage of each food item in populations collected in different host substrata, different habitat types and different distribution ranges. 94 M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98

Table 3 Results of ANOVA test on the influence of the distribution range (native vs introduced) and substratum (Bugula neritina vs Zoobotryon verticillatum for C. scaura and Eudendrium sp. for P. pusilla) in the percentage of the dominant food items.***P < 0.001. n.s. not significant.

Caprellid species Source of variation df %Detritus %Prey F vs.

MS FP MS FP

Caprella scaura Distribution range ¼ Ra 1 34.78 0.53 0.4661 0.01 0.9370 Res 0.01 Substrate ¼ Su 1 2022.28 31.02 0,0001*** 29.72 0,0001*** Res 34.51 Ra Su 1 34.78 0.53 0.4661 0.01 0.9370 Res 0.01 Residual 180 65.19 0.86 Cochran’s C-test C ¼ 0.51 (p < 0.01) C ¼ 0.51 n.s. Transformation None Ln (xþ1) Paracaprella pusilla Distribution range ¼ Ra 1 768.18 0.1966 955.68 Res 1.69 2.02 0.1594 Substrate ¼ Su 1 92.04 0.6535 18.18 Res 0.20 0.04 0.8452 Ra Su 1 1163.63 0.1129 768.18 Res 2.57 1.62 0.2066 Residual 84 453.38 474.16 Cochran’s C-test C ¼ 0.39 n.s. C ¼ 0.13 n.s. Transformation None None

Paracaprella pusilla and Caprella scaura, as with other fouling stealing the captured prey from the hydroid. Mayer (1882) and species, have the particularity that their dispersion usually takes MacKay (1945) stated that caprellids parasitize or eat hydroids, and place among artificial habitat, mainly ports, recreational marinas McDougal (1943) reported that caprellids invaded hydroid colonies and aquaculture structures. These habitats have similar character- for food and shelter and concluded that while the substratum was istics in different areas, including similar structures, fouling com- eaten to some extent, the major food sources were the food items munities or anthropogenic food resources. This implies that species occurring on the hydroid stems. that disperse within this habitat do not need to change their In the case of Caprella scaura, although it was found in a wide va- feeding strategies because the characteristics of the habitat type riety of substrata in its introduced range, it seems to prefer the bryo- remain similar between their native and introduced ranges, and the zoan Bugula neritina over other types of fouling substrata (Ros et al., availability of food items is always high. Although the total gut 2013b). This bryozoan is a suspension feeder which creates a current content must be carefully considered because it may be affected by bringing microscopic plankton and organic particles toward the ani- multiple factors that were not studied in this work, in general, mal. These currents may favour the intake of detritus by C. scaura. specimens of both species collected from artificial habitats had a In both cases, trophic relationships with its preferred substrata higher percentage of absolute gut content than specimens collected may favour the establishment and dispersal success of the species. from natural ones. This could reflect a higher availability of food source in the artificial than in the natural habitats. Only when the 4.4. Functional morphology of feeding species spread to natural areas, may a shift in their diet be neces- sary to adapt to the new environmental conditions, including the A relationship among feeding modes, preferred food and availability of their preferred food items or competition with other mouthpart morphology has been noted for several feeding special- taxa. In this crucial step of the invasion dynamics it is probable that ists among the amphipods (McCain, 1968; Caine, 1974; Mayer et al., P. pusilla, which shows a habitat-specific trophic ecology, may be 2008). Caine (1977) established that filter-feeder caprellids were more affected than C. scaura, which feeds widely and without re- those with molar and swimming setae but without mandibular gard of the different environments in which it inhabit. palps. These are the features of Caprella scaura, as well as the other species of the genus Caprella. However, Guerra-García and Tierno de 4.3. Trophic relationships between exotic caprellids and its Figueroa (2009) only found that, in caprellids, obligate predators preferred host substrata were characterized by the absence of molar process and swimming setae in the antennae 2. Caine (1977) previously established that We observed that individuals of Paracaprella pusilla collected caprellid predators were those with mandibular palps and molar from the hydroid Eudendrium sp. presented higher absolute gut processes but without swimming setae. P. pusilla has a rudimentary content than those collected from the bryozoan Bugula neritina. mandibular palp, the molar process is present but it is clearly less This may be due to a clepto-commensalist behaviour developed by developed than in C. scaura, and it lacks the swimming setae. This P. pusilla stealing captured prey from the polyps of the hydroid. This implies that, in any of the cases, its morphology is not specialized for peculiar trophic strategy was observed by Ros and Guerra-García an exclusive feeding strategy. In fact, P. pusilla is able to prey on other (2012) in P. pusilla in Southern Spain and previously by items, although it is probably less efficient in the intake of detritus Bavestrello et al. (1996) in other caprellid species (Pseudoprotella than C. scaura, which has a well-developed molar and swimming phasma and Caprella sp.) on Eudendrium glomeratum Picard, 1952 setae that create currents and act as a particle-collecting device. polyps. Alarcón-Ortega et al. (2012) studied the feeding habits of caprellids from the west coast of Mexico and found that Para- 4.5. Potential impacts on the recipient community caprella sp. associated with hydroids also showed a significant amount of small copepods in the digestive tract, supporting the As we show here, substantial predation on small crustaceans, idea of clepto-commensalism. Therefore, the presence of hydroids mainly harpacticoid copepods, supported a larger role in the tro- in their gut may be an accidental intake of polyps when P. pusilla is phic strategies of Paracaprella pusilla. Caine (1974), studying the M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98 95

Fig. 3. Diet preferences of Paracaprella pusilla based on the percentage of each food item in populations collected in different host substrata, different habitat types and different distribution ranges. 96 M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98

Table 4 Results of ANOVA test on the influence of the habitat (artificial vs natural) and substratum (Bugula neritina vs Zoobotryon verticillatum) in the percentage of the dominant food items in C. scaura and only on the influence of the habitat (artificial vs natural) in the percentage of the dominant food items in P. pusilla.*P < 0.05.

Caprellid species Source of variation df %Detritus %Prey F vs.

MS FP MS FP

Caprella scaura Habitat ¼ Ha 1 0.78 0.01 0.9171 7.03 0.84 0.3672 Res Substrate ¼ Su 1 94.53 1.33 0.2579 7.03 0.84 0.3672 Res Ha Su 1 175.78 2.48 0.1265 38.28 4.57 0.0413 Res Residual 28 70.87 8.37 Cochran’s C-test C ¼ 0.71 (p < 0.01) C ¼ 0.62 (p < 0.01) Transformation None None Paracaprella pusilla Habitat ¼ Ha 1 5824.26 6.78 0.0139* 6497.06 6.82 0.0136* Res Residual 32 27,494.11 953.31 Cochran’s C-test C ¼ 0.85 n.s. C ¼ 0.87 n.s. Transformation None None

predator behaviour of Paracaprella, asserted that: “It was never observed to fail to attack a suitably-sized organism within its reach”. 100 * With regard to the direct impact on the copepod community, small copepods employ a variety of strategies to maximize reproduction and survival in order to overcome likely substantial losses due to 80 predation and other factors (Turner, 2004). Webb and Parsons (1991) showed, in an experimental study, that exclusion of large epibenthic predators-disturbers had little effect on harpacticoid 60 copepod density. Based on this, it is unlikely that P. pusilla, even in Artificial high densities, may cause a significant impact on the copepod % Natural community. However, P. pusilla competes with the that 40 feed on copepods, such as fish larvae (Turner, 1984). In turn, cap- rellids constitute an important food item for adult fishes (Vázquez- Luis et al., 2010). 20 In the case of Caprella scaura, the large volume of organic * detritus in its gut contents suggests that it may play an important role as a vector for carbon transfer from detritus to top predators. Dense populations of C. scaura could both directly and indirectly 0 impact marine food webs by changing the quantity, form and Detritus Prey availability of these nutrients to other organisms. It is known that the introduced crayfish species Procambarus clarkii accumulates Fig. 4. Different percentages of detritus and prey in the gut content of Paracaprella heavy metals and other pollutants in its organs and body tissues pusilla associated to Eudendrium sp. between artificial and natural habitats from its native range (Brazil). Values are mean and standard error of the mean. and transmits them to higher trophic levels in freshwater habitats (Geiger et al., 2005). This also occurs with caprellid amphipods, especially detritivorous species. For example, caprellids have a high

2D Stress: 0.01

Paracaprella pusilla (Pp)

Caprella scaura (Cs) Pp-Eud

Cs-Zoo Cs -Zoo Pp-Eud Cs-Bug Cs-Bug Pp Cs -Bug -Zoo Pp-Bug Cs-Bug Pp-Eud

Habitat: Distribution range: Artificial Native (Brazil) Natural Introduced (Spain)

Fig. 5. Two dimensional MDS plot based on the diet of the two species in different habitats, ranges and substrata. Data are taken from the total values of Tables 2 and 3. Eud: Eudendrium sp.; Bug: Bugula neritina; Zoo: Zoobotryon verticillatum; Pp: Paracaprella pusilla; Cs: Caprella scaura. M. Ros et al. / Estuarine, Coastal and Shelf Science 139 (2014) 88e98 97 bioconcentration factor for TBT (Takeuchi et al., 2004), a toxic the European Union, and by the Consejería de Economía, Innova- compound that was used in antifouling paintings during the 1980s ción, Ciencia y Empleo, Junta de Andalucía (Project P11-RNM-7041). and early 1990s (Stewart, 1996). Given that C. scaura reaches high densities in the introduced areas (Guerra-García et al., 2011) and it Appendix 1. Capture locations, collection dates, habitats, is able to survive throughout the year (Ros et al., 2013b), it plays an substratum and caprellid species. A: artificial; N: natural; Pp: important role in the energy flow through food webs in introduced Paracaprella pusilla; Cs: Caprella scaura.

Country Locality Date Coordinates Habitat Substrate Caprellid species

BRAZIL Ilhabela (Sao Paulo) 04/10/12 23 460 S; 45 210 WA Bugula neritina Cs Ilhabela (Sao Paulo) 04/10/12 23 460 S; 45 210 WA Zoobotryon verticillatum Cs Paranaguá Harbor (Paraná) 22/11/12 25 300 S; 48 300 WA B. neritina Pp Paranaguá Harbor (Paraná) 22/11/12 25 300 S; 48 300 WA Eudendrium sp. Pp Sao Sebastiao (Sao Paulo) 02/10/12 23 460 S; 45 240 WN B. neritina Cs Sao Sebastiao (Sao Paulo) 02/10/12 23 460 S; 45 240 WN Z. verticillatum Cs Paranaguá Ilha do Mel (Paraná) 22/11/12 25 330 S; 48 180 WN Eudendrium sp. Pp SPAIN Cádiz 18/05/11 36 320 N; 6 170 WA B. neritina Cs Cádiz 18/05/11 36 320 N; 6 170 WA Z. verticillatum Cs Mallorca (Balearic Islands) 07/11/11 39 340 N; 2 380 WA Eudendrium sp. Pp Mallorca (Balearic Islands) 07/11/11 39 340 N; 2 380 WA B. neritina Pp ITALY Palermo 08/10/11 38 080 N; 13 220 EA B. neritina Cs Civitavecchia 29/05/12 42 050 N; 11 470 EA B. neritina Cs GREECE Iraklion (Creta) 18/05/12 35 200 N; 25 080 EA B. neritina Cs FRANCE Ajaccio (Corsica) 31/05/12 41 550 N; 8 440 EA B. neritina Cs MALTA Gzira 09/07/12 35 540 N; 14 290 EA B. neritina Cs

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