Eduardo D. Spivak

No longer the pristine confines of the world ocean: a survey of exotic marine species in the southwestern Atlantic

We conducted a comprehensive survey of existing knowledge about exotic marine organisms introduced to the southwestern Atlantic Ocean, including coastal and shelf areas of Uruguay and Argentina. This domain is equivalent to the so-called Patagonian Shelf Large Marine Ecosystem, and corresponds to two biogeographic provinces: warm-temperate (Argentine Province) and cold temperate (Magellanic Province). The search included species that can be confidently categorized as introduced (31) and cryptogenic species (46). We present a comprehensive picture of recorded introductions (the first for this region) and some prominent ecological consequences. Most coastal ecosystems between the La Plata River estuary and central Patagonia have already been modified, or are expected to be so in the short term. Five recent, human-mediated biological invasions have already had a significant ecological impact. A barnacle (Balanus glandula) belt has developed on all rocky shores where none was present 30 years ago, a macro-fouler (Limnoperna fortunei) and a reef-builder (Ficopomatus enigmaticus) have strongly modified estuarine ecosystems, Pacific oyster (Crassostrea gigas) reefs are expanding in shallow bays at a fast rate, and kelp (Undaria pinnatifida) is rapidly modifying nearshore benthic communities along the coasts of central Patagonia. At this point, it is uncertain how many of the cordgrasses (Spartina spp.) found in coastal salt marshes correspond to exotic forms. Only exposed sandy beaches appear to be free from the pervasive ecological impact of invasion by exotic species. Poor knowledge of the regional biota makes it difficult to track invasions.

Distribution and habitat preferences of two grapsid crab species in Mar Chiquita Lagoon (Province of Buenos Aires, Argentina)

Cyrtograpsus angulatus andChasmagnathus granulata (Grapsidae) are the two dominant decapod crustacean species in the outer parts of Mar Chiquita Lagoon, the southernmost in a series of coastal lagoons that occur along the temperate Atlantic coasts of South America. Distribution and habitat preferences (water and sediment type) in these crab species were studied in late spring. There is evidence of ontogenetic changes in habitat selection of both species. Recruitment ofC. angulatus takes place mainly in crevices of tube-building polychaete (Ficopomatus enigmaticus) “reefs” and, to a lesser extent, also in other protected microhabitats (under stones). In the latter, mostly somewhat larger juveniles were found, suggesting that these are used as a refuge for growing individuals. Adults are most frequently found on unprotected muddy and sandy beaches.C. angulatus was found in all parts of Mar Chiquita Lagoon, including freshwater, brackish, and marine habitats.C. granulata, in contrast, was restricted to the lower parts of the lagoon, where brackish water predominates and freshwater or marine conditions occur only exceptionally. It showed highest population density on “dry mud” flats and inSpartina densiflora grassland, where it can build stable burrows and where high contents of organic matter occur in the sediment. Such habitats are characterized by mixed populations of juveniles (including newly settled recruits) and adults, males and females (including a high percentage of ovigerous). Unstable “wet mud” as well as stony sand were found to be inhabited by chiefly adult populations, with only few ovigerous females. In “dry mud” flats, the proportion of males increased vertically with increasing level in the intertidal zone, showing a significantly increasing trend also in their average body size. These observations may be explained by higher resistance of males, in particular of large individuals, to desiccation, salinity, and temperature stress occurring in the upper intertidal. However, an opposite, or no such, tendency was found in the distribution of ovigerous and non-ovigerous females, respectively. With increasing distance from the water edge, salinity increased and pH decreased significantly inC. granulata burrows, whereas temperature showed no consistent tendency within the intertidal gradient. A highly significant linear relationship (r=−0.794; P<0.001) between salinity and pH in water from crab burrows is described. This regression line is significantly different from one that had been observed in water from the lagoon, indicating consistently lower pH values at any salinity level in burrow water. This is interpreted as a result of crab and/or microbial respiration.

Hatching rhythms and dispersion of decapod crustacean larvae in a brackish coastal lagoon in Argentina

Mar Chiquita, a brackish coastal lagoon in central Argentina, is inhabited by dense populations of two intertidal grapsid crab species,Cyrtograpsus angulatus andChasmagnathus granulata. During a preliminary one-year study and a subsequent intensive sampling programme (November–December 1992), the physical properties and the occurrence of decapod crustacean larvae in the surface water of the lagoon were investigated. The lagoon is characterized by highly variable physical conditions, with oligohaline waters frequently predominating over extended periods. The adjacent coastal waters show a complex pattern of semidiurnal tides that often do not influence the lagoon, due to the existence of a sandbar across its entrance. Besides frequently occurring larvae (exclusively freshly hatched zoeae and a few megalopae) of the two dominating crab species, those of three other brachyurans (Plathyxanthus crenulatus, Uca uruguayensis, Pinnixa patagonica) and of one anomuran (the porcellanidPachycheles haigae) were also found occasionally. Caridean shrimp (Palaemonetes argentinus) larvae occurred in a moderate number of samples, with a maximum density of 800·m−3. The highest larval abundance was recorded inC. angulatus, with almost 8000°m−3. Significantly moreC. angulatus andC. granulata zoeae occurred at night than during daylight conditions, and more larvae (statistically significant only in the former species) during ebb (outflowing) than during flood (inflowing) tides. In consequence, most crab zoeae were observed during nocturnal ebb, the least with diurnal flood tides. Our data suggest that crab larvae do not develop in the lagoon, where the adult populations live, but exhibit an export strategy, probably based upon exogenously coordinated egg hatching rhythms. Zoeal development must take place in coastal marine waters, from where the megalopa eventually returns for settlement and metamorphosis in the lagoon. Significantly higher larval frequency ofC. granulata in low salinities (≤12‰) and at a particular sampling site may be related to local distribution patterns of the reproducing adult population. Unlike crab larvae, those of shrimp (P. argentinus) are retained inside the lagoon, where they develop from hatching through metamorphosis. They significantly prefer low salinity and occur at the lagoon surface more often at night. These patterns cannot be explained by larval release rhythms like those in brachyuran crabs, but may reflect diel vertical migrations to the bottom. It is concluded that osmotic stress as well as predation pressure exerted by visually directed predators (small species or life-cycle stages of estuarine fishes) may be the principal selection factors for the evolution of hatching and migration rhythms in decapod larvae, and that these are characteristics of export or retention mechanisms, respectively.

Effects of reduced salinities on development and bioenergetics of early larval shore crab, Carcinus maenas

The shore crab, Carcinus maenas L. (Portunidae), is a coastal and estuarine species, which can live and reproduce under brackish water conditions; freshly hatched larvae have been observed in the field at salinities below 15 parts per thousand. In the present laboratory study, the tolerance of hypo-osmotic stress was experimentally investigated in early larvae of a marine (North Sea) population of C. maenas reared at four different salinities (15, 20, 25, 32 parts per thousand). Two and 4 days after hatching, the Zoea I larvae were moult-staged microscopically, and their rates of respiration and growth (changes in dry weight, W, carbon, C, nitrogen, N, and hydrogen, H) were measured. Survival and development were monitored until the megalopa was reached: 15 parts per thousand did not allow for development beyond the first zoeal stage, while metamorphosis to the megalopa was reached at salinities greater than or equal to 20 parts per thousand. At 20 parts per thousand, development was significantly delayed and mortality enhanced as compared with 25 and 32 parts per thousand. Rates of growth and respiration decreased during exposure to reduced salinities less than or equal to 25 parts per thousand. Hence, the suppression of growth could not be explained as a consequence of enhanced metabolic losses per larva. Instead, a partial C budget indicates that the Zoea I larvae suffered from decreased capabilities of assimilating ingested and subsequently converting assimilated matter to tissue growth. Net growth efficiency (K-2, C-based) was at 25 and 32 parts per thousand initially high (> 60% during the postmoult and intermoult stages of the Zoea I moult cycle), but decreased during the later stages (down to less than or equal to 30% in premoult). An inverse pattern of C partitioning was observed at less than or equal to 20 parts per thousand, with initially low K-2 values (less than or equal to 21% during the first 2 days of the moult cycle), and a later increase (up to greater than or equal to 46% in premoult). Thus, larval growth was initially suppressed under conditions of reduced salinity, but this was later (during premoult) partially compensated for by an increase in C assimilation and K-2. Our observations indicate that Zoea I shore crab larvae react during the late stages of their moulting cycle less sensitively against reduced salinities than during postmoult and intermoult. This suggests that the transition between moult cycle stages C and D-0 may be a critical point for effects of hypo-osmotic stress, similarly as already known in relation to effects of nutritional stress. Negative effects were found also when freshly hatched Zoea I shore crab larvae were exposed only transitorily (for 24-72 h) to 20 parts per thousand, with significantly lower rates of survival, development, growth, respiration, and K-2. These effects increased with increasing duration of initial exposure to reduced salinity.

Experimental studies on predation and cannibalism of the settlers of Chasmagnathus granulata and Cyrtograpsus angulatus (Brachyura: Grapsidae)

The grapsid crabs Chasmagnathus granulata and Cyrtograpsus angulatus are considered as key species within the benthic communities of estuaries and brackish coastal lagoons in the southwestern Atlantic region. In controlled laboratory experiments, we studied the intensity of interspecific predation as well as intra- and intercohort cannibalism in setllers in relation to refuge availability, predator characteristics (species, size, sex, nutritional state), and the presence or absence of an alternative food source (Artemia nauplii). In both species, the intensity of intracohort cannibalism among recently settled crabs (instars I and II, “settlers”) was low, with ca. 5% mortality during 48 h experimental observation periods. Larger juveniles and adults of both species, by contrast, preyed heavily on the settlers. Predation was significantly reduced when refuges were available for the settlers. Hunger of the predators enhanced in general the predation rate. In the presence of alternative food, the consumption of settlers was significantly reduced. In C. granulata, adult females ate more settlers than the males, probably as a consequence of differences in the morphometric traits of their chelae. Cannibalism and predation by juvenile and adult crabs may play an important role in the regulation of recruitment success for both species and hence, in the structure of estuarine benthic communities.

Seasonal and interpopulational variability in fecundity, egg size, and elemental composition (CHN) of eggs and larvae in a grapsoid crab, Chasmagnathus granulatus

Reproductive traits at the beginning and the end of the annual reproductive season were compared between two populations of the intertidal crab Chasmagnathus granulatus living in ecologically contrasting habitats: (1) Mar Chiquita (MC) (37°45′S, 57°19′W), a highly productive estuarine coastal lagoon with strong salinity fluctuations. (2) San Antonio Bay (SA) (40°46′S, 64°50′), a physically stable but less productive coastal marine environment. Number, size, and elemental composition (CHN) of eggs and larvae differed significantly between populations. Regardless of the season, more but smaller eggs and larvae were produced in MC, while eggs and larvae from SA revealed higher dry mass and C/N ratios indicating higher lipid content. A latitudinal temperature gradient cannot explain these patterns, suggesting that other environmental factors including salinity, quality or quantity of benthic food sources and productivity may be responsible. In both populations, fecundity and biomass per egg were higher at the beginning as compared to the end of the reproductive season. As a consequence, the reproductive effort was consistently maximal at the beginning of the season. At MC, also variability was found between two successive years. Intraspecific (both interpopulational and seasonal) variations in reproductive and developmental traits may be important for the formation of physiologically different metapopulations along the wide geographic range of C. granulatus.

Population structure of the South American Estuarine crab, Chasmagnathus granulatus (Brachyura: Varunidae) near the southern limit of its geographical distribution: comparison with northern populations

AbstractCrabs are among the most conspicuous and ecologically important invertebrates of the large intertidal zones that characterize estuarine and protected coastal areas in temperate regions. The habitat, population structure and breeding cycle of Chasmagnathus granulatus (Brachyura: Varunidae), a semiterrestrial burrowing crab endemic to the warm temperate coasts of the Southwestern Atlantic, were studied in San Antonio Bay (Argentina), near the southern limit of its range. San Antonio Bay has no freshwater input, winter is relatively colder, and summer warmer, than northern habitats of this species. Crabs lived both in vegetated and unvegetated zones, but density and sex ratio varied among dates and zones. The maximum observed density was 136 crabs/m2 , the maximum carapace width (CW) was 32 mm (males) and 29.8 mm (females), ovigerous females were found only in November and January, and the smallest ovigerous female measured 17 mm CW. The population structure, spatial distribution, and recruitment pattern of C. granulatusdid not differ between San Antonio Bay and northern habitats. The higher density, smaller maximum size and shorter reproductive cycle observed in San Antonio cannot be atributed to changes associated with a latitudinal cline and other factors, such as thermal amplitude and food availability, need to be studied.

Cangrejos estuariales del Atlántico sudoccidental (25º-41ºS) (Crustacea: Decapoda: Brachyura)

RESUMEN. Se compara la fauna de decapodos y las caracteristicas ambientales de varios estuarios y lagunas costerasdel Atlantico sudoccidental, ubicados entre los 25 y los 41°S: Baia de Paranagua, Manguezal de Itacorubi, Lagoa dosPatos (Brasil), Laguna Castillos (Uruguay), Rio de la Plata (Uruguay-Argentina), Laguna Mar Chiquita y Bahia Blanca(Argentina). Se revisa la informacion sobre historia natural de las especies de cangrejos (Crustacea: Brachyura) que loshabitan. El numero de especies de cangrejos desciende bruscamente entre Itacorubi y Lagoa dos Patos, junto a la dismi-nucion de la temperatura minima del agua. Las bajas temperaturas invernales tienen un efecto directo sobre la fisiologiade muchas especies, pero tambien estan relacionadas con la desaparicion de los manglares y la variedad de microhabitatque estos generan. Sin embargo, el efecto de la temperatura no es suficiente para explicar algunos aspectos relacionadoscon la distribucion de las especies y sus historias de vida.

The effects of temperature and salinity on larval development of Armases rubripes Rathbun, 1897 (Brachyura, Grapsoidea, Sesarmidae), and the southern limit of its geographical distribution

Abstract The southernmost stable population of Armases (=Metasesarma) rubripes (Brachyura, Grapsoidea, Sesarmidae) is found in Montevideo, Uruguay, in the northeastern coast of the Rio de la Plata estuary. Isolated individuals have seldom been collected in the southwestern coast of this huge estuary. Since pelagic larvae are primarily responsible for the dispersion of A. rubripes, and crab larvae are generally less tolerant than adults to extreme environmental conditions, we tested the survival and intermolt period of zoeae in different combinations of salinity (10, 20, and 30 psu) and temperature (16 and 20 °C). These salinity and temperature conditions are usually found in the estuary and adjacent waters during spring and summer. We found that the survival rate of the larvae increased and they developed faster at 30 psu and 20 °C. It is unlikely that larvae from the Montevideo population of A. rubripes could be transported south and westward due to the hydrographic conditions of the region. The Rio de la Plata seems to function as a biogeographic barrier to A. rubripes, and probably to other crab species as well. However, this barrier is not absolute: it hinders, but does not entirely prevent, the dispersal of larvae.

Variation in early developmental stages in two populations of an intertidal crab, Neohelice (Chasmagnathus) granulata

Duration of embryonic development, egg size, larval size at hatching, and starvation tolerance of the first zoeal stage were studied in an intertidal crab from the southwestern Atlantic, Neohelice (formerly Chasmagnathus) granulata. These reproductive traits were quantified comparing (a) two populations living in ecologically contrasting coastal habitats in Argentina, a brackish lagoon, Mar Chiquita, MC vs. an open marine habitat near San Antonio, Patagonia, SA, (b) beginning vs. end of the reproductive season, and (c) two temperatures during egg development (18 vs. 27°C). Eggs in an early stage of embryonic development were in both populations larger at the beginning than at the end of the season, and were consistently larger in the SA population. These size differences persisted through larval hatching, independent of the temperature during embryogenesis. At 18°C, eggs produced at the beginning of the season developed in both populations more rapidly than those from the end of the reproductive season, while the opposite trend was observed at 27°C. The stage duration of the zoea I was in both populations shorter at the beginning as compared to the end of the season. The nutritional flexibility of the zoea I stage was compared using as indices the point-of-reserve-saturation (PRS50) and the point-of-no-return (PNR50). The PRS50 was consistently lower in larvae from SA than in those from MC. In the MC population, this index was lower at the beginning than at the end of the season, while no significant seasonal difference was observed in larvae from SA. The PNR50 varied between temperatures of embryonic development and populations, showing also significant interactions between all three factors. The PRS50 was on average lower, and the PNR50 was higher, than values previously reported for N. granulata, suggesting a stronger nutritional flexibility in the larvae used in the present study. Our results indicate significant intraspecific variability among separate populations, seasonal variation, and carry-over effects of environmental conditions prevailing during the embryonic phase, all of which may affect the performance of the larval phase.