First record of an epibiosis between the sand crab Emerita analoga (Stimpson, 1857) (Decapoda: Hippidae) and the mussel Semimytilus algosus (Gould, 1850) (Bivalvia, Mytilidae) in southern Peru
Coastal zones of the Humboldt Current Upwelling System (HCUS) are composed both of rocky and sandy beaches inhabited by macrozoobenthic communities. These show oscillating changes in the dominance of species; the abundance of the sand crab Emerita analoga is linked to phases of the El Niño Southern Oscillation (ENSO). The biogenic surfaces of these crabs serve as substrate for opportunistic colonizers. This study is the first record of an epibiosis between E. analoga and the rock mussel Semimytilus algosus, detected at a southern Peruvian sandy beach. Mussels fouled a wide size-range of adult E. analoga (7.3%) but they themselves belonged to small-size classes. The largest S. algosus was 17.4 mm in length. Highest permanence of epibionts was found on larger sand crabs (maximum between 24 and 27 mm). Significantly more mussels were found on the ventral surface (39.4%) compared to 10 other surface areas of the sand crab. Possible benefits and disadvantages of the observed epibiosis for both the basibiont and the epibiont are discussed.
KeywordsHumboldt Current Upwelling System Epibiosis Fouling Semimytilus algosus Emerita analoga
The coastal Humboldt Current Upwelling System (HCUS) is one of the most productive marine ecosystems (Mann and Lazier 1991; Escribano et al. 1997; Marín et al. 2001). The system is fuelled by upwelling of nutrients, which stimulate the primary and secondary production (Escribano et al. 1997; Marín et al. 2001). Coastal zones of the HCUS consist of rocky as well as sandy beaches colonized by a diverse macroinfauna of invertebrates contributing to a high biomass (Soto 1985; Jaramillo et al. 1993; Arntz and Fahrbach 1996). There are many studies on the patterns of macrofaunal zonation in exposed sandy beaches of the coastal upwelling system (e.g. Jaramillo et al. 1993, 2001; Jaramillo and McLachlan 1993), showing that changes in beach morphodynamic result in significant community responses of the intertidal macroinfauna. Communities of sandy beaches of south and central Peru show clear fluctuations of dominant species such as the surf clams Mesodesma donacium and Donax marincovichi, and the sand crab Emerita analoga. The main reasons for these are natural climate variability as the El Niño Southern Oscillation (ENSO) (Tarazona et al. 1985; Arntz et al. 1987; Arntz and Fahrbach 1996) and overexploitation.
The sand crab E. analoga (Crustacea, Anomura, Hippidae) is a widespread and abundant decapod inhabiting exposed sandy beaches of the Pacific coast (e.g. Contreras et al. 1999), and is a characteristic specie of the swash zone (Jaramillo et al. 1993, 2001; Contreras et al. 1999). It can appear in high abundance forming aggregations at certain water temperatures, food availability and beach morphodynamics (Perry 1980; Dugan 1994; Jaramillo and McLachlan 1993; Contreras et al. 1999). The combination of substrate generalist characteristics and the unique orientation and swimming ability of E. analoga may be a key to its high abundance and wide distribution in the intertidal zone of exposed sandy beaches (Dugan et al. 1994, 2000). The hard carapace of this crab offers free substratum for species colonizing hard structures (Wahl 1989; Gili et al. 1993).
For metamorphoses and settlement the free-living larvae of sessile hard bottom invertebrates are highly dependent on the availability of a suitable substratum (Sebens 1985; Gili et al. 1993). The coastal area of northern Chile and southern to central Peru is dominated by soft bottom habitats, while rock substratum is scarce. Biogenic surfaces can also serve as settlement substrates resulting in epibiosis, a close association between two different species: a basibiont (the substrate organism) fouled by an epibiont (organism growing attached to a living surface; Wahl 1989). Host species reported from sandy beaches are mainly molluscs and crustaceans (Conover 1979; Warner 1997; Olabarría 2000), fouled by diverse sessile invertebrates. Such an association usually includes both benefits and disadvantages for epi- and basibiont (Wahl 1989; Gili et al. 1993), which have a more prominent effect under strong physical environmental conditions such as wave exposure and currents (Jackson 1977; Wahl 1989; Olabarría 2000). In southern Peru we observed that E. analoga was fouled by the rock mussel Semimytilus algosus, a common inhabitant of the low rocky intertidal fringe in central Chile, distributed between Ecuador and ChiloeIsland (approximately 42°S, Caro and Castilla 2004). The aim of this study was to describe this epibiosis and to discuss possible effects for both the host and the epibiont.
Materials and methods
Sampling and analysis
Sand crab E. analoga fouled by the mussel S. algosus were collected in the intertidal zone along the beach. Individuals of E. analoga covering the whole size range were sampled within a time period of 5 min each in two 100 m wide areas. The abundance of E. analoga in the study area was determined using a cylindrical corer (10 cm in diameter). Individuals were fixed in 5% formalin. Thereafter individuals were measured (length of carapace) to the nearest 0.1 mm and observed under a binocular microscope in order to detect epibionts. Epibiotic mussels were identified and counted, their position on the basibiont was recorded and their length was measured. S. algosus was found attached to 11 different surface areas of E. analoga (see also Fig. 5): (1) ventral side, (2) right side of carapace, (3) inferior left maxilliped, (4) area between first and second pereiopod, (5) anterior right edge of carapace, (6) dactylus of first pereiopod, (7) superior pereiopod left, (8) left side of carapace, (9) superior pereiopod right, (10) dorsal carapace, (11) area between coxae and carapace. Images of fouled areas were taken using a digital camera (Canon G3—Power shot) and a binocular microscope (Carl Zeiss) with 230 magnification.
Biogenic substrates are commonly used as settling substrates by hard-bottom colonizers, especially in dynamic soft bottoms where no or only a few other substrates are available. This especially holds true for our study site, a long highly exposed beach without solid rock. Hard bottom is very scarce over a long distance of coastline, apparently resulting in a high competition pressure for settling surfaces. Crustacean carapaces and shells of molluscs of different species were reported as potential substrates for colonizers in such soft-bottom habitats (Conover 1979; Gili et al. 1993; Olabarría 2000). However, an association between the sand crab E. analoga and the rock mussels S. algosus has not yet been reported. The latter dominates exposed rocky intertidal communities in the low and middle latitudes of Pacific South America (Tokeshi and Romero 1995) and is recognized as an important primary colonizer in the HCUS (Tarazona et al. 1985; Tokeshi and Romero 1995). The larval phase of this mussel species varies from 17 to 20 days. Recruitment of S. algosus occurs throughout the year with major peaks in summer and, secondarily, winter months (June–August), showing interannual changes during EN (Navarrete et al. 2002).
The sand crab E. analoga substituted the surf clams (Tarazona et al. 1985; Arntz et al. 1987) and became available as settlement substrate for the pioneer mussels. As a consequence mussels were observed fouling a wide size range of adult E. analoga. Most epibiotic mussels belonged to a correspondingly small-size class of probably young individuals. The highest permanence of epibionts was found on larger basibionts suggesting that bigger hosts offer more shelter and stability for the mussel to protect it from physical factors such as wave exposure. The evolutionary response of sessile basibionts to a potential epibiosis includes three classes of adaptations: tolerance, avoidance and defence (Wahl 1989). In crustaceans the mechanic defence such as the periodic renewal of the carapace due to moulting and the ‘sanding’ in dynamic high energy sandy beaches might regulate the colonization rate (Wahl 1989; Gili et al. 1993). Thus large-sized sand crabs might be more susceptible to fouling as the molt interval is longer and the crabs inhabit zones with more stable conditions.
Defence may be costly while tolerance entails both benefits and disadvantages for epi- and basibiont. According to Wahl and Mark (1999), specific and obligate epibionts are rare. Consequently, the majority of described associations are classified as facultative. The association between E. analoga and S. algosus probably involves a complex network of cost-benefit factors for the two species. In soft bottoms the opportunistic settlement of S. algosus on E. analoga may be the only opportunity for successful larval metamorphosis. The percentage of fouled E. analoga (7.3%) appears important considering the density of sand crabs (about 65 ind m−2) in the study area. The abundance of E. analoga varies between 10 and 85 ind m−2 (Arntz et al. 1987) and can reach maximum values of 111.6 ind m−2 before EN (Tarazona et al. 1985). In southern Chile even much higher values of 1675 ind m−2, related to temporal variability in recruitment, were reported (Contreras et al. 1999).
Mainly juvenile mussels were attached to the crabs. Individuals of S. algosus in northern and central Chile (lat 30°) reach a maximum size exceeding 70 mm (Gonzáles et al. 1980; Tokeshi and Romero 1995), are hermaphroditic with mature gametes during the entire year (Gonzáles et al. 1980), and may obtain sexual maturity at 20 mm (Gallardo 2001). In the present study the maximum size of epibiotic S. algosus was a little smaller (17.4 mm). However, our study site was 1300 km north of the former study area and it is possible that in low latitudes the bivalves reach sexual maturity in smaller size classes (according to Thorson 1950). S. algosus on E. analoga are unlikely to commonly reach size necessary for reproduction. However, small mussels may colonize other substrates later on by detaching from the substrate and drifting elsewhere while larger individuals may undergo a lateral movement (Tokeshi and Romero 1995). Under favourable conditions and when more biogenous substrates for settlement are available (e.g. surf clams M. donacium), S. algosus may reach higher densities (Arntz 1987; Arntz and Fahrbach 1996), and epibiosis may facilitate the dispersal and contribute to gene flow of the rock mussel populations even more prominently.
Due to increased drag and mass the epibiont is likely to reduce the growth of the crabs (Wahl 1997) and might impact their migration behaviour. Furthermore, mechanical attachment of larger epibionts occasionally damages surfaces of the basibiont (Witman and Suchanek 1984; Wahl 1989).
In top-down controlled systems, epibiosis can strongly influence community dynamics, affecting many epibiont–basibiont–consumer interactions (Wahl 1989; Wahl et al. 1997; Laudien and Wahl 1999, 2004). In the western Baltic, for instance, the sea star Asterias rubens preys preferably on unfouled mussels (M. edulis) and the predation pressure decreases significantly when the mussels are fouled by hydrozoan and algae. This beneficial effect of fouling is known as associational resistance (Laudien and Wahl 1999, 2004). However, in the case of the rock mussel–sand crab association, the opposite effect (‘shared doom effect’, Laudien and Wahl 1999) might occur when epibiotic individuals of larger size reduce the ability of E. analoga to escape from predators by increasing mass, reducing motility, and ultimately prolonging the burrowing time during the tidal migration (Dugan et al. 2000). A future study of the burrowing behaviour under predation pressure might give a deeper insight into the cost and benefits of this epibiosis between S. algosus and E. analoga.
Sampling was conducted during the fieldwork of the FIP project 2001-24 carried out by the Group of Ecology and Management of Resource (ECOLMAR). We especially thank Pablo Araya for his assistance in the field. Thanks are also due to Ivan Hinojosa and Sebastian Boltaña who helped taking the digital photos. Wolf Arntz provided underwater pictures of S. algosus–M. donacium associations. We are grateful to Renate Kuchta who helped with Fig. 8 and to Domingo Lancellotti and Heinz-Dieter Franke who gave valuable comments on an earlier version of the manuscript. This study was conducted in the frame of the EU project CENSOR (Climate variability and El Niño southern oscillation impacts for natural resources and management).
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