Integrative and Comparative Biology Advance Access originally published online on June 15, 2006
Integrative and Comparative Biology 2006 46(5):615-622; doi:10.1093/icb/icl010
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Phenotypic links in complex life cycles: conclusions from studies with decapod crustaceans
Sección Oceanología, Facultad de Ciencias Iguá 4225, 11400 Montevideo, Uruguay
Correspondence: 1E-mail: lgimenez{at}awi-bremerhaven.de
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I review studies on decapod crustaceans to draw conclusions about the importance of effects of past environmental conditions on development, phenotype, performance, and survival in animals. I consider 3 critical points of the life cycle: the allocation of reserves into eggs, the hatching of larvae, and metamorphosis from the larval to the juvenile phase. Biomass allocated to eggs varies among females as a response to changes in environmental conditions. These variations are propagated to the larval stages, influencing the biomass at hatching, subsequent larval developmental pathways, and survival during periods of limited starvation. Suboptimal conditions experienced by embryos increase the loss of mass during embryogenesis; size or biomass of the juvenile is either positively or negatively correlated with initial biomass. Positive correlations may be the normal pattern; negative correlations occur when individuals hatched with low initial biomass follow developmental pathways that lead to increased biomass at metamorphosis. In estuarine crabs, salinity experienced by embryos leads to salinity acclimation in early larval stages. Phenotypic links originate as transgenerational effects that propagate to the juvenile stages. There are least 3 types of effects: disruption of physiological processes; direct adaptive responses; and indirect consequences of adaptive mechanisms. All types appear within a species; they are produced as a response to a single environmental factor. Variability in phenotype remains latent and is expressed in terms of survival according to the environmental conditions experienced by a particular stage. The fate of individuals is thus affected by interactions between their immediate developmental processes and their environmental history.
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Introduction |
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"You could not step twice into the same river; for other waters are ever flowing on to you."
Eraclitus
In recent years a growing body of literature has suggested that environmental conditions may affect traits of individuals at early life phases and lead to variation in survival and reproduction of organisms with complex life cycles. This contrasts with classic attempts to explain the performance and survival of organisms as a consequence of present environmental conditions. Environmentally induced variation in traits in an early life phase (for example embryo) is carried over to the next life phase (for example larva or juvenile). In terms of survival, that variation remains latent at early stages, but is expressed later in development or at maturity. Most of the research on these phenotypic links or "carry-over effects" comes from laboratory experiments (Kunisch and Anger 1984
; Pechenik and others 1998; Beckerman and others 2003; Räsänen and others 2005; Giménez and others 2004). Theoretical research also has suggested that phenotypic links lead to cohort effects, which in turn affect the dynamics of the populations through changes in the strength of density-dependence (Beckerman and others 2003). These population models differ from those using the logistic equation or stage/age structured matrix models as they consider that life-history traits may vary in time (see Beckerman and others 2002). Other theoretical consideractions suggest an important influence on connectivity among populations, settlement, and recruitment (McCormick 1998; Giménez 2003, 2004). Previous recruitment models have not considered the importance of these phenotypic links to explain recruitment limitation. Both experimental and theoretical advances call for field work evaluating the importance of natural variability in the traits of individuals and its consequences for performance. The available information suggests that phenotypic links are important to explain natural variability in survival and reproduction (Phillips 2002; Jarrett 2003; Altwegg and Reyer 2003; McCormick and Hoey 2004; Marshall and Keough 2005). Further advances may be achieved by integrating experimental and field research (Podolsky 2003).
At the present stage of development of this field it is appropriate to evaluate the existing information. Phenotypic links might have been observed for a long time but not recognized as such because they were treated as "noise," or disregarded in order to study other processes. Now such "noise" may turn out to be an interesting "signal."
Here, I review the existing data on phenotypic links that occur during the life cycle of decapod crustaceans. General characteristics of the life cycle and early development of decapod crustaceans were summarized by Anger (2001). Briefly, for the reviewed species, embryos are carried by the females for several weeks, so embryonic development occurs in the parental habitat. After hatching, larvae are released into the water with larval development usually passing through 2 or more zoeal stages plus a decapodid (= megalopa in brachyurans). Decapodids metamorphose to a first juvenile stage.
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Phenotypic links in decapod crustaceans |
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Strong phenotypic links, as the consequence of seasonal and temperature variations, were found throughout early life of the spider crab Hyas araneus (Kunisch and Anger 1984
). This species is characterized by large eggs, 2 zoeal stages, and a megalopa (see Anger 1990, 1991, 2001 for reviews). Kunisch and Anger (1984) found that duration of larval development decreased through the hatching season while size at metamorphosis increased. Individuals hatching early in the season took more time to complete larval development and they metamorphosed to smaller crabs. Interestingly, growth effects from conditions experienced by embryos were still strong after the larval phase, during early juvenile development. As in larval stages, duration of juvenile development to the fourth juvenile stage also decreased throughout the season. Higher temperatures during embryogenesis led to lower larval growth rates and to smaller size at metamorphosis. Variations in the size at metamorphosis were still present at the fourth juvenile stage, 
2 months after the end of larval life.
Indeed, temperature may be one of the main factors affecting variability in size or biomass at hatching. In another species, Cancer magister, Shirley and colleagues (1987) noted that size at hatching varied with latitude from Alaska to California, with increasing size toward the higher latitudes. They also showed that lower temperature during embryogenesis led to larger size at hatching, suggesting that latitudinal patterns may be produced at least in part by the variation in temperature experienced by embryos. Temperature experienced by embryos may affect the size or biomass at hatching in various ways. For instance, temperature may change either the instantaneous rate of biomass loss or the total loss of biomass by changing the duration of embryonic development.
While in brachyuran crabs, such as H. araneus, seasonal and temperature variations affect larval size, in shrimps, such as Crangon crangon, they excert stronger effects, influencing the developmental pathways followed by larvae (Criales and Anger 1986; Linck 1995; Paschke 1998; Paschke and others 2004). In C. crangon there is seasonal variation in the size and biomass of eggs, with maxima in winter and minima in summer; accordingly, larvae from summer eggs hatch with lower biomass than do those from winter eggs (Paschke 1998). The hatching pattern is bimodal, with peaks in late winter and late summer (Anger 2001). Caridean shrimps, such as C. crangon, are characterized by a variable development; due to genetic differences or as a consequence of varying environmental conditions, individuals may follow alternative developmental pathways differing in morphology and number of stages (Anger 2001). In the case of C. crangon, seasonal changes in egg size affect the developmental pathway (Criales and Anger 1986; Linck 1995). Larvae from winter eggs develop to the first juvenile stage through a smaller number of larval stages than do those hatching from summer eggs (Linck 1995; Fig. 1). For instance, larvae reared at 12°C develop through 4–5 stages if they hatch from winter eggs, but 6 stages are required when hatching occurs from summer eggs. There were also differences in the developmental rate per instar, with larvae from winter eggs developing faster than those from summer eggs (Linck 1995). Zoeae I from winter eggs tolerate longer periods of starvation than do those from summer eggs: zoeae I from winter eggs exhibited a longer point of no return (PNR) and shorter point of reserve saturation (PRS) than did those from summer eggs (Paschke and others 2004). The PNR is the minimum initial starvation period after which larvae do not recover from nutritional stress. Starvation period beyond the PNR leads to irreversible damage in the hepatopancreatic cells and prevents accumulation of lipids and production of ecdysone (Anger 2001). The PRS is the minimum initial feeding period after which larvae become independent of food for the rest of the moulting cycle. Beyond the PRS, morphogenetic processes are triggered and proceed independently of food sources (Anger 2001).
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Strong and complex funtional links occur also in estuarine crabs in response to salinity. Experiments with the crab Chasmagnathus granulatus have uncovered a rich diversity of links from the moment of egg laying to the end of juvenile life (Fig. 2). Giménez and Anger (2001)
found that females of the crab C. granulatus exposed to low salinities laid eggs of larger size and higher biomass. Low salinity increased the loss of biomass during embryogenesis in C. granulatus, negatively affecting the biomass of freshly hatched larvae. Survival of zoea I was correlated with biomass at hatching if larvae experienced waters of 15–32
(Giménez and Anger 2003). Also initial larval biomass affected survival under limited food conditions (Giménez 2002): zoeae I with higher biomass showed a longer PNR. Thus, low salinities during embryogenesis lead to low survival of larvae developing at 15–32. If, however, zoea I encountered lower salinities (5–10) high survival was restricted to the first zoeal stage and then only if the embryos were exposed to salinities of 15–20 (Charmantier and others 2002; Giménez and Anger 2003); otherwise survival was very low. There is therefore a short-term acclimation process during embryonic development that enhances larval survival at low salinity. If zoeae I experienced a moderatley low salinity (20), acclimation also reduced PRS, that is increased starvation tolerance (Giménez 2002). In this case, acclimation favored a rapid accumulation of reserves during a brief feeding period. The above-described effects of salinity on larval survival were found earlier in the mud crab Rhithropanopeus harrisii (Rosenberg and Costlow 1979; Laughlin and French 1989a). Biomass at hatching was, in this species, positively correlated with the salinity experienced by the embryos, suggesting that osmotic stress increased biomass loss. Embryonic acclimation to low salinity was reflected in the patterns of larval survival.
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Also here, environmental conditions experienced by embryos codetermined the larval developmental pathway and affected the biomass of late larval and early juvenile stages. In C. granulatus, larval biomass at advanced stages (zoea IV, megalopa) depended on the initial larval biomass (Giménez and Torres 2002
). The larval development of C. granulatus is variable, with two alternative developmental pathways consisting of either 4 or 5 zoeal stages before the megalopa. When individuals followed the short pathway, the biomass of the megalopae and of juvenile stage-I were positively correlated with the biomass at hatching; thus, early variability in biomass propagated through the larval stages (Giménez and Anger 2001; Giménez and others 2004; see R. Podolsky and A. Moran, unpublished data, for definitions). However, individuals followed the long pathway more frequently when the biomass at hatching was low. These individuals continued growing during the zoea V stage and metamorphosed to larger megalopae and juveniles than did those following the long pathway. The pattern of early variability was reversed during the larval phase, leading to a partial compensation of size after metamorphosis (Giménez and Torres 2002; Giménez and others 2004).
A further kind of phenotypic link in crustaceans is related to chemical cues accelerating metamorphosis (reviewed in Forward and others 2001; Gebauer and others 2003). In C. granulatus, the absence of a chemical cue, associated with muddy substrates or with adult crabs, reduced the size at settlement and survival of the first juvenile stage (Gebauer and others 1998, 1999). There are only a few studies on that topic in decapod crabs (Gebauer and others 2003).
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Discussion |
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Past environmental variation interacts with developmental and physiological processes to determine the present phenotype of an organism. Phenotype interacts with the present environment to determine survival. This aspect has been recently emphasized by evolutionary biologists as it defines the context within which natural selection operates (see Kaplan and Phillips 2006
). From the point of view of physiology, the study of phenotypic links opens ways of understanding organismal functioning by considering the individual "life story." For ecology, it introduces us to overlooked processes that may co-influence patterns of distribution and abundance (Beckerman and others 2003; Giménez 2004). These "life stories" are, after all, a source of life-history variation occurring at ecological time-scales and thus relevant for ecology. We see from the reviewed information that through the life cycle (1) phenotypic links start as transgenerational effects, transmittted by the parents; (2) these continue through a series of diverse effects; and (3) they are ultimately manifested in terms of survival in a context-dependent manner. Below, I discuss each of these 3 aspects.
Transgenerational effects: sometimes there is no new beginning
Some phenotypic links appear with life itself, as transgenerational maternal effects, and propagate through the life cycle. Transgenerational effects are demostrated by variable and adaptive maternal allocation of reserves into eggs. These propagate in different ways throughout the larval and juvenile stages.
Transgenerational effects are common in terrestrial and aquatic plants and animals (Agrawal and others 2000; Mondor and others 2005). The evolutionary importance of transgenerational effects have been reviewed in several papers (for example Mousseau and Fox 1998). The importance of population dynamics has been already stressed (Beckerman and others 2002). As delayed life-history effects they may produce considerable temporal variation in population abundance.
Diverse effects occur throughout the life cycle
From the available information it is clear that there are at least 3 kinds of effects. The first is a stress effect: environmental variability produces physiological stress on a developmental stage, leading to effects in the traits of subsequent stages. This is the case of the effect of salinity on the loss of biomass taking place during embryogenesis in C. granulatus. The same may occur with R. harrisii at different salinities and perhaps with H. araneus at different temperatures. Such effects may be widespread among species occupying heterogeneous environments, as suggested by a study on a euryhaline barnacle (Qiu and Qian 1999). Most likely larval dispersal and the colonization of suboptimal habitats lead to variability in initial larval biomass.
The second type of effect consists of direct adaptive responses to environmental variation, in the sense that the response has an adaptive value (Gothard and Nylin 1995). These responses buffer environmental effects on survival. They should involve a series of physiological mechanisms following an environmental signal. The patterns of reserve allocation to eggs as a response to seasonal conditions (C. crangon) or salinity (C. granulatus) are examples of adaptive effects. Providing larger reserves to eggs in winter may lead to a reduced larval developmental rate and to increased starvation tolerance in C. crangon early in the year, when larvae hatch and planktonic food is scarce (Paschke and others 2004). Also, providing more reserves in eggs at low salinity may compensate for increased loss of biomass during embryogenesis at low salinity. Both strategies enhance survival of early stages in heterogenous environments (Giménez 2003). In addition, they allow for an expansion in time of the reproductive season (Paschke and others 2004) and an expansion of the distributional range to colder latitudes or to sites with low salinity.
Embryonic acclimation to salinity also falls within the direct adaptive response to environmental conditions; in this case an "acclimation state" is carried to the larval phase. Acclimation involves an increase in osmoregulatory capacity on zoea I in C. granulatus (Charmantier and others 2002) most likely through biochemical and cellular changes in the transport tissues located in the branchiostegites. The adaptive value of the propagation of the acclimation state lies in the fact that salinities experienced at the end of embryonic development will be approximately the same as those experienced by zoea I. Later, larvae leave low-salinity areas and develop in coastal waters of higher salinity. A theoretical examination of the importance of acclimation under field conditions was conducted recently (Giménez 2003). Several populations are located along a large-scale salinity gradient produced by the Río de la Plata and the Atlantic Ocean in South America. Zoeae I are thus released in waters varying greatly in salinity. Under such a scenario, larvae released in low-salinity areas will successfully reach waters of moderate to high salinities. Further field studies (Bas and Spivak 2003) showed that the acclimation capacity varied among individuals from different estuarine zones. Acclimation to salinity also occurred in R. harrisii and may be found in other estuarine especies that release larvae in estuarine waters. Embryonic acclimation to other factors, such as temperature, may also be widespread.
The third type is an indirect effect of an adaptive response to environmental conditions. This is exemplified by the case of environmental stress operating on early larvae and leading to alternative pathways and differential juvenile size and biomass in C. granulatus. Alternative pathways are seen as a general response to stress (low food quality, low salinity) during early larval development. Knowlton (1974) proposed it as a strategy that prioritized survival and growth over morphogenetical processes when biomass fails to reach a certain threshold. Thus, subsequent changes in size at metamorphosis cannot be interpreted as a direct adaptive response to benthic conditions; they are, at least in part, a by-product of an adaptive response to larval conditions. It is expected that this indirect effect is spread among species developing through alternative developmental pathways such as shrimps and grapsid crabs (Anger 2001).
Manifestation of effects in terms of survival is context-dependent
Changes in the physiological state of individuals are propagated throughout the life cycle, but its manifestation in terms of survival is context-dependent. For instance, in C. granulatus zoea I, developing in seawater, the initial larval biomass plays a significant role in survival. At low salinity, acclimation plays the most important role. In the latter case variability in allocation of biomass into eggs may not be as important as variability in osmoregultory capacity. Also in C. granulatus, differential survival of crabs from short versus long developmental pathways occurs as a consequence of starvation, not osmotic stress (Giménez and others 2004). In both cases, trade-offs between egg size and egg number may switch on and off depending on the environmental conditions experienced by the offspring (see Marshall, this volume, for implications; Giménez in press: for C. granulatus).
Another example is the time of starvation during larval development. During the molting cycle, crab larvae develop through an initial phase of high growth rate and accumulation of reserves, followed by another phase in which development proceeds independently of food (Anger 2001). In consequence, larvae of decapod crustaceans may be characterized as sensitive to initial conditions. This is clearly shown by the experiments with C. crangon and C. granulatus (Giménez 2002; Paschke and others 2004): early starvation produced a stronger effect on duration of development and on survival than did late starvation. Sensitivity to initial conditions in crustaceans is also suggested by experiments manipulating food availability (Hentschel and Emlet 2000; Howard and Hentschel 2005).
Finally, effects may change among populations, as suggested by studies with C. granulatus (Bas and Spivak 2003) and R. harrisii (Laughlin and French 1989b). In this case the context may be altered by different environmental conditions selecting for genotypes varying in their capacity for plastic responses. Thus, for C. granulatus from the lagoon of Mar Chiquita, characterized by variable salinities, selection should favour flexible physiological mechanisms that allow for successful survival regardless of the salinity experienced by the embryos (Bas and Spivak 2003). This selective force may not be so strong in San Antonio Bay, where there are rather constant salinities (Bas and Spivak 2003). There, trade-offs driven by other selective processes may lead to the elimination of such flexible physiological mechanisms.
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Perspectives |
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The present review covers information from a small number of publications. While I am aware that not all published data may be covered, it is still clear that there is a need to incorporate the role of phenotypic effects and development in field and laboratory studies.
Field studies
In the field one needs to begin with the study of effect of interactions between pre-hatching and post-hatching on survival and development. As shown here, these interactions are complex and set the context for further interactions, between pre-metamorphic and post-metamorphic conditions and events.
We also need to develop a framework to evaluate the combined effects of transport processes and other variables on benthic recruitment. In the marine habitat, functional links may affect recruitment; presettlement processes may be seen as influenced by a combination of density-mediated effects that impinge upon larval supply and trait-mediated effects that affect mortality after settlement (Giménez 2004). Density-mediated effects have been related to variability in transport and availability of larval food (Menge and others 1997). The occurrence of functional links may lead to an increasing importance of food availability, temperature, or salinity since they affect the larval phenotype and produce the trait-mediated effects.
Both trait-mediated and density-mediated effects on recruitment success may be seen from the point of view of the match–mismatch hypothesis developed for fish larvae (Cushing 1996; see also Chick and Van den Avyle 1999). Since variablity in benthic recruitment has been related to several factors affecting food availability (see Menge and others 2003), the success of recruitment should depend on whether there is a match between larval periods and the periods of food avilability. Mismatches may lead to either low larval survival or low quality of settlers resulting in high post-settlement mortality.
In addition, trait-mediated and density-mediated effects obligue us to see recruitment in a wider framework, as the consequence of the combined effect of transport and other variables, such as food availability, temperature, and salinity, on survival and traits of settlers. Within this framework, spatial and temporal variability in oceanographic conditions may lead to cases of synergistic (Menge and others 1997), antagonistic, or decoupled (Menge and others 2003) effects of these variables on recruitment. Synergistic (or antagonistic) effects consist in favourable tranport conditions being possitively (or negatively) correlated with for example food availability. If there is decoupling, recruitment may be explained by either transport processes (as in supply-side theory) or by for example food availability (as in the match–mismatch hypothesis). Hopefully, we will see in coming years an evaluation of the combined importance of density- and trait-mediated effects in recruitment studies.
Laboratory studies
Laboratory studies are important in understanding the causes of natural variation in traits and survival of individuals. It is necessary to estimate how plastic the phenotype is for different genotypes, that is, what is the "scope for plasticity"? As stressed earlier (Giménez 2004), metamorphosis or other developmental processes may act as a "filter" so that only a narrow range of phenotypic variability is carried into the juvenile stages. The characteristics of this filter may change among genotypes. Evidence from experiments with species with variable development suggests that the characteristics of the developmental pathways have a genetic basis (Anger 2001). In genotypes with only a few pathways, the size at metamorphosis may be less plastic. This remains to be tested by future experiments.
Experiments are needed to understand relationships between size and fitness. As shown by experiments with C. granulatus the larger is not always the better (see also George 1999). The larger individuals, originated from the long pathway, resist starvation for a longer time, but they metamorphose later and develop more slowly. In the long run, the advantages of a larger size may be overrun by the advantages of growing faster.
In summary, the available data about decapod crustaceans tell us that there is a great diversity of phenotypic links originated by environmental effects interacting with developmental mechanisms. Throughout the life cycle of the decapod crustaceans these phenotypic links are interacting with each other, affecting survival of larvae in advanced larval stages and juveniles in a context-dependent manner. Thus, in heterogenous environments, particular "life stories" may arise within a population. Phenotypic links need to be incorporated into field studies as they may help to reach a better understanding of recruitment processes and population dynamics. Incorporating the evaluation of these links to a research program may enlighten us about the causes of temporal and spatial variability in distribution and abundance of organisms.
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Acknowledgements |
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This review was made possible through a kind invitation by Dr R. Podolsky, Dr A. Moran, and the Society for Integrative and Comparative Biology. Comments and discussions with colleagues at that meeting greatly helped to develop the ideas exposed in this paper. The author appreciates the help and support given by Dr K. Anger and colleagues at his laboratory at the Marine Station of Helgoland. The author also appreciates support and discussions with G. Charmantier and M. Charmantier-Daures. The author's research was funded by DAAD and Alexander von Humboldt Foundation from Germany, CSIC, and PEDECIBA from Universidad de la República of Uruguay.
Conflict of interest: None declared.
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2Present address: Biologische Anstalt Helgoland, Foundation Alfred Wegener Institute for Polar and Marine Research, 27498 Helgoland, Germany
From the symposium "Integrating Function over Marine Life Cycles" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida.
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