Neotropical Biology and Conservation 6(3):143-155, september-december 2011 © by Unisinos - 10.4013/nbc.2011.63.01

An overview of studies on trophic in the marine environment: Achievements and perspectives

Um panorama sobre os estudos de ecologia trófica em ambientes marinhos: Resultados e perspectivas

Martin Lindsey Christoffersen1* [email protected] Abstract Classical approaches to trophic ecology of marine species has focused on trophic struc- Maria Elisabeth de Araújo2 ture, trophodynamics, dominant and , maturity, energy [email protected] transfer, and anthropic effects. A recent breakthrough for evaluating the structure of com- munities has been the application of phylogenetic methods to ecology. This Joaquim Olinto Branco3 recent approach is known as community phylogenetics. Although this perspective is still [email protected] not common in trophic studies, phylogenetic methods promise new insights into the old ecological question on how communities are assembled in time. Integrating phylogene- tics and ecosystem function creates the possibility of predicting ecological consequen- ces of shifts in a changing world. Once we understand the structure and functioning of the ecosystem in a historical context, we should be able to avoid human or natural disturbances that draw a system away from its state of maximum complexity.

Key words: trophic structure, trophodynamics, keystone species, ecosystem maturity, energy transfer, anthropic effects, community phylogenetics.

Resumo

Abordagens clássicas para estudos de ecologia trófica de species marinhas focam a es- trutura trófica, a trofodinâmica, espécies dominantes e espécies-chave, maturidade de ecossistemas, transferência de energia, e efeitos antrópicos. Um avanço recente para avaliar a estrutura de comunidades foi a aplicação de métodos filogenéticos à ecologia de comunidades. Esta abordagem recente é conhecida como filogenia de comunida- des. Embora esta perspectiva ainda não seja comum em estudos tróficos, métodos filogenéticos prometem novas abordagens à velha questão ecológica de como entender a organização de comunidades ao longo do tempo. A integração de filogenia com o funcionamneto de ecossistemas cria a possibilidade de prever as consequências de alterações na biodiversidade num mundo em mudança. Uma vez entendida a estrutura e o funcionamento do ecossitema num contexto histórico, deveremos poder evitar alte- 1 Universidade Federal da Paraíba, De- rações naturais ou humanas que tendem a desviar o sistema ecológico do seu estado partamento de Sistemática e Ecologia, Cidade Universitária, 58.059-900, João de complexidade máxima. Pessoa, PB, Brazil. 2 Universidade Federal de Pernambuco, Palavras-chave: estrutura trófica, trofodinâmica, espécies-chave, maturidade de ecossis- Departamento de Oceanografia, Av. temas, transferência de energia, efeitos antrópicos, filogenia de comunidades. Arquitetura, s/n, Cidade Universitária, 50.740-550, Recife, PE, Brazil. 3 Centro de Ciências Tecnológicas da Terra e do Mar, Universidade Vale do Itajaí (UNIVALI), Rua Uruguai, 458, Cx. P 360, CEP 88302-202, Itajaí, SC, Brazil. * Corresponding author Martin Lindsey Christoffersen, Maria Elisabeth de Araújo, Joaquim Olinto Branco

Introduction trophic functions in coastal systems between basal and top species. Chains represent the best way the communi- involving more than six species are Most studies on marine macrobenthic ties can adapt to exploit the existing rare (Hutchinson, 1959; Pimm, 1982; communities have been conducted resources as a response to physical Cohen et al., 1986). The knowledge in north temperate regions. Tropical gradients (Carvalho et al., 2010). of diet is important for the establish- and subtropical macrobenthos is less Marine biodiversity is higher in ben- ment of its nutritional needs and of known, especially the South Atlantic thic rather than pelagic systems. The the interactions with other organisms fauna (Santos and Pires-Vanin, 2004). best way to conserve marine diversity (Albertoni et al., 2003). W. Odum and In relation to temperate regions, tropi- is to conserve and landscape Heald (1975) used effective trophic cal systems are typically dominated diversity in the coastal area. Feeding level to group various taxa into com- by smaller species (Froese et al., 2004, relationships may cause invasions, mon feeding categories. The emphasis 2005). There is a reduced in extirpations, and population fluctua- in all of these studies has been at the low latitudes, compared to middle tions of a species that dramatically ecosystem level (Christian and Lucz- and high latitudes (Chardy and Cla- affect other species within a variety kovich, 1999). vier, 1988). In the tropical zone this of natural (Williams et al., The analysis of the trophic structure kind of study is more complex since 2002). Macrobenthic communities are of benthic communities is also a use- a large number of species are present now used worldwide as ful way to determine the main energy and are frequently represented by only (Diaz and Rosenberg, 1995; Belan, flow at the ecosystem level. Most ec- a few individuals. The high biological 2003; Carvalho et al., 2006; Cardoso ological research has relied on trophic diversity obscures the recognition of et al., 2007). groups as a classification scheme for specific food webs responsible for Food webs, descriptions of who eats defining functional diversity (Micheli the larger part of the whom in , provide com- and Halpern, 2005). analy- (Paiva, 1993; Santos and Pires-Vanin, plex yet tractable depictions of bio- sis has also been a well-documented 2004). Trophic structure of tropical diversity, species interactions, and tool to achieve a fisheries ecosys- fish communities in particular con- ecosystem structure and function tem approach and to understand the trast with those from temperate re- (Dunne et al., 2002). Strong and ecosystem under various scenarios gions in terms of more efficient use of weak trophic links are responsible (Abarca-Arenas et al., 2007; Pauly et relatively low-quality food resources for ecological dynamics among di- al., 1998, 2000). (Harmelin-Vivien, 2002; Floeter et verse assemblages of species. The use Both abiotic (temperature, salinity, al., 2004; Ferreira et al., 2004). of trophic groups to characterize the substrate) and biotic factors (compe- Coastal ecosystems are relatively rich role of macrobenthos in marine com- tition, ) play a role in shap- in nutrients and play a significant role munities is advantageous since it in- ing macrobenthic communities (An- in the development of many species corporates estimates of macrobenthic germeier and Winston, 1998). Food of economic interest. Studies on the community structure, and assesses or availability plays an important role feeding habits of macroinvertebrates infers community functioning (Gaston in the structure of coastal commu- and demersal fish, even those of a et al., 1995; Boaventura et al., 1999). nities in addition to abiotic factors descriptive character, provide basic On the other hand, feeding patterns of (Vaslet et al., 2010). Predation func- information for understanding the macrobenthic organisms have been tions in limitation (Verity, trophic relations of species (Rocha et frequently used to distinguish ecologi- 1998). Trophic interactions are one al., 2007; Gasalla and Soares, 2001). cal zones (Pearson and Rosenberg, of the determinants of distribution Coastal systems such as lagoons, sea 1987; Boaventura et al., 1999; Dias and of organisms (Duarte grass banks and estuaries are char- et al., 2001). Knowledge of both web and Garcia 2004). Trophic ecology of acterized by high eco-physiological structure and interaction strengths is a macrobenthic communities in estuar- capacities of biological communities key to understanding how ecological ies may be used not only to infer com- against extremely varying environ- communities function (Berlow et al., munity function, but may also provide mental conditions, in space and time 2004). insights into community responses (Villanueva et al., 2006; Bascompte, The feeding roles of species are thus following disturbances (Gaston et 2009; Ings et al., 2009). The insta- important tools for the evaluation of al., 1998). Trophic structure has thus bility of the coastal zone affects the the structure and functioning of eco- become one of the primary ways by benthic community, determining the systems (Krebs, 1989). Species occur which ecologists organize communi- patterns of distribution and density at top, intermediate and basal trophic ties and ecosystems (Christian and and the trophic relationships among levels (Williams and Martinez, 2000). Luckzkovich, 1999). the species (Santos and Pires-Vanin, Food chains tend to be short, typi- In this paper we overview the accom- 2004). The existence of gradients of cally with only three or four kinds plishments of classical approaches to

144 Volume 6 number 3  september - december 2011 An overview of studies on trophic ecology in the marine environment: Achievements and perspectives the study of trophic structure in ma- Assigning of feeding types to each Luczkovich et al. (2003) defined rine environments, and then point out species is sometimes ambiguous and trophic role similarity as species that present developments and future di- not consensual (Chardy and Clavier, play the same structural roles, even rections in community phylogenetics. 1988). The general importance of if they are not directly consuming omnivory in regulating predator-prey the same prey or if they do not share Macrobenthos interactions and in predicting the rela- the same predators. This information tive importance of indirect predator is useful for measuring the trophic Temporal and spatial patterns of mi- effects was analyzed by Posey and roles of species in food web models, crohabitat used by fishes and decapods Hines (1991). The omnivory index for measuring similarity in trophic in a Louisiana estuary were shown to represents the variance of the effective relations of two or more species, for determine overall community structure trophic levels of a ´s preys comparing food webs over time and in the system (Baltz and Jones, 2003). (Christensen and Pauly, 1992). Most across geographic regions, for ag- The role of fish predation in determin- consumers feed on several trophic gregating taxa into trophic groups ing the benthic community structure levels, as shown by omnivory indices that reduce complexity of ecosystem was specifically studied by Gilinsky (Manickchand-Heileman et al., 1998). feeding relations without obscuring (1984). In coastal lakes of West Africa, Complex predator-prey interactions network relationships, and for pre- and piscivore trophic guilds prevail within an estuarine benthic dicting the outcome of predator-prey had most species (Adite and Winemill- community. The diversity of trophic interactions in experimental studies. er, 1997). Spatial and temporal separa- levels of prey fed upon by a predator Aggregations of biological species tion in the distribution and/or dietary increases with the index value. Organ- on the basis of trophic similarity have preferences of fish in salt-marshes in isms at higher trophic levels seem to been called trophospecies and are South Carolina was found to probably feed over a broader range of levels the basic units of study in food web reduce the potential for resource com- than do organisms at lower levels. and ecosystem research (Yodzis and petition (Allen et al., 1995). Also, as increases, the Winemiller, 1999). energy flow of an average compart- Group-specific trophic signatures have Trophic structure ment at any trophic level decreases been establisehd as plots of number of (Christian and Luckzkovich, 1999). species per trophic level. Froese et al. Trophic interactions are web-like, A species’ trophic group is a determi- (2004) used these signatures to iden- with the strongest flows occurring nant of that species’ role in the energy tify similarities and discrepancies be- in the lower part of the trophic web transfer within the assemblage. Chang- tween taxonomic groups and ecosys- (Manickchand-Heileman et al., 1998). es in lead to changes tems. Trophic signatures are similar Nets have multiple connections and in functional diversity (Micheli and for ecosystems previously known to organisms take food from different Halpern, 2005). Food webs in nature share major features, and different for trophic levels, denoting opportunistic have multiple, reticulate connections dissimilar ecosystems. Trophic sig- generalists (Polis and Strong, 1996). between a diversity of consumers natures may be useful tools for better Trophic levels range from and resources. Such complexity af- understanding the roles that different to predators (Froese et al., 2004). Top fects web dynamics (Polis and Strong, groups of organisms play in different species are those which prey upon 1996). Trophic groups in coastal ecosystems (Froese et al., 2004). One other species but are not themselves habitats in Portugal were assigned to type of trophic signature is generated preyed upon. Intermediate species four distinct categories (filter feeders, by a plot of species frequency in rela- have both prey and predators. Basal , herbivores, and carni- tion to their number of trophic links species have predators but no prey vores) (Boaventura et al., 1999). Six (Williams et al., 2002). (Briand and Cohen, 1984). trophic categories were recognized A feeding is defined as a set of Primary producers and are for mangrove shoreline fish commu- organisms that exploit food resources placed in trophic level 1. Herbivores nities in Caribbean lagoons: piscivo- in a similar intake mechanism, inde- and detritus consumers are level 2. The rous, , 1 and 2, pendently of their phylogenetic rela- remaining predators are placed in level herbivores, and (Vaslet tionships. Feeding guilds of a benthic 3 and up (W. Odum and Heald, 1975). et al., 2010). Demersal communities community can be broadly divided Trophic levels higher than five rarely in the Gulf of Mexico were organized into deposit feeders, suspension feed- exist in nature (Pimm, 1982). However, into three guilds: ichthyophagous, ers, herbivores, carnivores, and om- second and third-level predators typi- carcinophagous, and omnivorous. In nivores (Cheung et al., 2008). Deter- cally exploit a wide range of prey, from general, juvenile stages showed a nar- mining the trophic guilds of fishes and herbivores to other second or third-lev- rower trophic spectrum than adults macroinvertebrates in coastal habitats el predators (Froese et al., 2004). (Torruco et al., 2007). should greatly improve the develop-

Neotropical Biology and Conservation 145 Martin Lindsey Christoffersen, Maria Elisabeth de Araújo, Joaquim Olinto Branco

ment of future network models of food structure among the different seasons of responses are potentially an impor- webs by providing an objective proce- the year (Abarca-Arenas et al. 2007). tant force in stabilizing communities. dure for aggregating trophic groups Trophodynamic aspects of fish in Yuca- The term ¨redundant species¨, thus, (Luczkovich et al., 2002). Multiple tan have been studied, for example, by conveys an inaccurate image of the trophic levels have been identified in Vega-Cendejas et al. (1987). potential importance of weak inter- soft-bottom communities (Commito actors and should thus be abandoned and Ambrose, 1985). Linkage den- Dominant and (Navarrete and Menge, 1996). Fol- sity, the number of trophic links per keystone species lowing Yodzis and Winemiller (1999), species, once thought to be constant, we prefer the use of trophic similar- is now known to increase with the is the appropriation of ity or trophospecies for these trophic number of species in the web (Cohen potential niche space of certain sub- equivalences. et al., 1990). ordinate species by other dominant A keystone predator crops down the The existence of gradients of trophic species and so can be manifested most dominant competitor from reaching functions in these systems may rep- clearly only within a trophic level. In a competitive equilibrium. Thus, pre- resent the best way the communities other words, a producer cannot domi- dation constitutes an important factor can adapt to exploring resources as a nate a or predator be- that disturbs the trend of response to physical gradients (Can- cause the immediate sources of their and curbs it, counteracting dominance cela da Fonseca et al., 2001). Duarte et energy and inorganic nutrients are not (Raghukumar and Anil, 2003). Key- al. (1990) questioned whether trophic overlapping. Dominant species tend stone predation demonstrated that un- group patterns of macrobenthos repre- to be generalists (McNaughton and weighted link structure by itself is not sent a good tool to understand macrob- Wolf, 1970). a good predictor of species and popu- enthos communities. Clustering spe- It may sometimes be interesting to lation dynamics (Paine, 1969, 1974, cies by trophic group overlooks well identify those species that play an 1980). For example, Gasalla et al. known variation in the functional roles important role in the ecosystem, also (2010) evaluated the keystone role of of species within a trophic guild. But known as keystone species (Dunne et the squid Loligo plei in a southwestern a species´ trophic group, in combina- al., 2002; Luczkovich et al., 2003). Atlantic ecosystem. The studied squid tion with its size, can be a determinant Keystone species are those that have represents an important link between of that species´ role in energy transfer large impacts on communities or eco- pelagic and demersal energy pathways, within a food web and in controlling systems out of proportion to their with high indices of keystoneness. other species within the assemblage abundance (Power et al., 1996). The idea that communities may be (Micheli and Halpern, 2005). Species that have both large abun- dominated by a few keystone species Finally, trophic box models of aquatic dances and large impacts are con- has a long history in ecology (Mills et ecosystems have been established by sidered dominant species instead of al., 1993). Yet McCann et al. (1998) Christensen and Pauly (1993). Such keystones. Species with few trophic and Berlow (1999) provide an alterna- models were applied to coastal fish connections that have large effects tive viewpoint, based on weak trophic communities in the Gulf of Mexico on community structure may act as interactions. For the intertidal habi- (Arreguín-Sánchez et al., 1993), and the structural equivalent of keystone tat, Menge et al. (1994) propose that for a coastal system in northwest species, whereas species with many it is variation in interaction strength Africa (Diallo et al., 2003). trophic linkages may be more con- that determines community structure, ceptually similar to dominant species questioning the usefulness and gener- Trophodynamics (Dunne et al., 2002). Jordan et al. ality of the keystone concept. Because (1999) and Jordan (2001) proposed a we expect all complex ecosystems Ecosystem models have not always method to identify a keystone species to be structured similarly, this type been successful for predicting the using weighted trophic networks. of analysis could help conservation future development of complex eco- In keystone-dominated systems, spe- managers identify connected keystone logical systems (Ulanowicz, 1993). cies other than the keystone species species that should be the focus of Attempts have therefore been made have only minor, if any, effects on the conservation efforts (Parrott, 2010). to develop structural dynamic mod- rest of the community, and thus might els – which change parameters, even be cited by some as ¨redundant spe- Ecosystem maturity species composition, over time (Jør- cies¨. However, after loss of a key- gensen, 1986, 1988, 1992). stone species, previously ¨redundant¨ Biodiversity and community structure The trophic dynamic concept in ecology species can partially compensate for are now recognized to be important was established by Lindeman (1942). the reduced predation and adopt a determinants of ecosystem function- Food web dynamics showed a variable major role in the altered system. Such ing. High diversity leads to greater

146 Volume 6 number 3  september - december 2011 An overview of studies on trophic ecology in the marine environment: Achievements and perspectives community stability and productiv- glue that binds natural communities was first established by Paine (1969). ity (Raghukumar and Anil, 2003). together (McCann et al., 1998). The diversity-stability debate con- And changes in species diversity lead Thus, the more trophic links that a tinued with May (1973), with early to changes in functional diversity species has to other species in a food multi-species models, and may help (Micheli and Halpern, 2005). web, the more potential it may have identify the role of weak or positive Predation can maintain high local spe- to affect community structure (Dunne interactions in community structure cies diversity if the predator consumes et al., 2002). Community stability (McCann, 2000). The interacting a competitively dominant prey spe- will increase as the number of links webs should provide more accurate cies (Paine, 1966, 1971; Menge and in a food web increases (MacArthur, characterizations of the complex Sutherland, 1987). In this situation, 1955). Highly connected communi- structural signatures of ecosystems. the predator will have a fundamental ties will tend to be more robust to Recent research continues to confirm influence at the community level by species losses (Dunne et al., 2002). the presence of temporal, spatial, and structuring interactions between spe- On the other hand, secondary extinc- structural signatures that share com- cies and reducing the impact of each, tions occur due to removal of highly mon characteristic patterns across all thereby permitting coexistence that connected species. Unfortunately, the types of complex ecosystems. Ecologi would not occur in the absence of the degree to which taxonomic and func- cal complexity often represents a link predator (Calil et al., 2009). Predators tional diversity are correlated is un- to concepts such as ecological resil- commonly show a variety of trophic known for most ecosystems (Naeem, ience and ecological integrity (Levin, strategies and prey selectivity (Brög- 2002). Given the high diversity that 1999; Harris, 2007). ger and Penchaszadeh, 2008). characterizes tropical regions, the The degree of complexity of an eco- Food-web structure mediates dramatic study of dominant species has been system is correlated with its health or effects of biodiversity loss, includ- a widespread research strategy. This integrity, both of which very likely ing secondary and cascading extinc- approach can identify important eco- increase a system´s resilience and ro- tions. Food webs are more robust to logical interactions among members bustness (Loreau et al., 2001; Hooper random removal of species than to of a diverse demersal fish community, et al., 2005). Functional and struc- selective removal of species with the acting both as sources of information tural redundancy increases system most trophic links to other species. of the members themselves, and of complexity in space and time, and Robustness increases with food-web other species with similar behavior provides increasing robustness and connectance but appears independent (Sánchez-Gil et al., 2008). tolerance to (Carlson and of and omnivory. Re- The relationships of species richness Doyle, 2002). moving species with few trophic con- and other measures of complexity to Stability has been based typically on nections generally has little effect on ecosystem properties need to be fur- local stability analysis. Local stabil- biodiversity loss. Thus, the number of ther explored, such as in network to- ity does not guarantee persistence of species removed affects ecosystems pology and related food-web studies food webs in stochastic environments. differently depending on the trophic (Solé and Montoya, 2001; Williams Global stability and permanence could functions of species removed (Dunne et al., 2002; Dunne et al., 2002; Mon- be better criteria of community per- et al., 2002). toya and Solé, 2002). To determine sistence. The relationship between We should expect decline in diver- food web complexity, four statistics stability and complexity of food webs sity to accelerate the simplification are commonly used: species richness, remains a central issue in theoreti- of ecological communities. Diversity number of trophic species in the food cal ecology. May (1972) suggests that can be expected, on average, to give web, links per species, and omnivory complexity reduces stability. Many rise to ecosystem stability. Weakly (Dunne et al., 2002). efforts have been made towards incor- interacting species stabilize commu- Many have tried to define stability (May, porating structural features of real food nity dynamics by dampening strong, 1975; Rutledge et al., 1976; Pimm, webs into the pool of community ma- potentially destabilizing consumer- 1979, 1984; Johnson, 1981; Mauri- trices of dynamic models (DeAngelis, resource interactions (E. P. Odum, ello, 1983), buffer capacity (Jørgensen, 1975; Yodzis, 1981; Pimm, 1982). 1953). Decreasing biodiversity will be 1990) and resilience of communities Communities with more omnivory accompanied by increases in average and ecosystems (Berryman, 1983). But links have more prevalent permanent interaction strengths within ecosys- the whole idea of energy flow ruling paths and communities of high con- tems, and a concomitant decrease in ecosystem interaction has also been nectance are more ready to reassem- ecosystem stability. Simplified com- questioned on the basis of chaos theory ble themselves (Law and Blackford, munities are consequently more vul- (Månsson and McGlade, 1993). 1992; Law and Morton, 1993). Thus, nerable to invasion (McCann, 2000). The relationship between trophic complex communities may also be Weak interactions may thus be the complexity and community stability less vulnerable to disturbance than

Neotropical Biology and Conservation 147 Martin Lindsey Christoffersen, Maria Elisabeth de Araújo, Joaquim Olinto Branco

simple ones. Within stochastically ecosystem (Parrott, 2010). Complex- versely, restoration efforts may help assembled food webs, complex food ity may serve as a fourth indicator of the system to self-organize towards webs are less likely to be permanent the degree of maturity or organization a state of higher complexity (Parrott, than simple webs; in other words, in of an ecosystem (Müller, 2005). Com- 2002), once we understand the struc- these simulation analyses, perma- plexity of natural ecosystems increas- ture and functioning of the ecosystem. nence actually decreases as food web es with maturity (Parrott, 2010). The For successful , complexity increases (Chen and Co- relationship between respiration and we need to take into account not only hen, 2001). production represents a final measure prey and predators of a target species, Food webs of high connectance are of the maturity of the ecosystem (E. P. but also their role in an overall eco- shown to rebuild themselves more Odum, 1969). system context (Christensen, 1996). readily than those of low connectance, Trophic relations of fish in northwest- and therefore recover more readily Energy transfer ern Atlantic were studied to determine from disturbance (DeAngelis, 1975; the role that predation plays in deter- Law and Blackford, 1992). Connect- Transfer of energy from one trophic mining ecosystem structure and the ance remains surprisingly constant, level to another is only about 10% ef- possible long-term effects of various while the fractions of top and basal ficient. Trophic relationship studies of fisheries exploiting regimes (Bowman species decreased, and the fraction of macrobenthos show that primary pro- et al., 2000). intermediate species increased (Mar- duction of the overlying water is not a Trophic structure of macrobenthic as- tinez et al., 1999). Species redundan- limiting factor for benthic production semblages is closely linked to envi- cy (Naeem, 1998), or species diversity (Joydas and Damodaran, 2009). Pop- ronmental characters and serve as in- (Naeem and Li, 1987), which we refer ulations with higher effective trophic dicators of environmental conditions to as trophic similarity, or trophospe- levels would be expected to contribute (Gaston and Nasci, 1988), permitting cies, enhance ecosystem reliability. less to the energetics of the ecosystem the assessment of anthropic perturba- Ecosystem development is seen by than those with lower levels. tion in marine and estuarine systems E. P. Odum (1969) as a process that The links between the primary pro- (Gaston et al., 1998). A common ap- involves structural changes in the sys- ducers and the top consumers are of- proach to assess risks to ecosystem tem that are orderly, directional and ten poorly understood. Aggregation of health is to identify stressors and their therefore predictable. The develop- species into trophic guilds is required potential effects through the use of in- ment is to culminate in a stable sys- for network analysis of most, if not dicators (Fisher et al., 2001). tem with maximum biomass and/or all natural ecosystems (Christian and Macrobenthic communities are now information content. In this climactic Luckzkovich, 1999). used worldwide as bioindicators (Diaz system widespread symbiotic inter- Trophic relations follow a pyramid of and Rosenberg, 1995; Belan, 2003). actions will tend to optimize energy flows (Lindeman, 1942). The efficien- Community structure, trophic func- utilization (Christensen, 1995). Un- cy of trophic transference diminishes tional analysis and several biotic met- fortunately, the lack of general predic- gradually towards the higher trophic rics should be tested in order to assess tion seriously impedes the maturation levels, due to the increase in the rate their effectiveness in discriminating of ecology as a scientific discipline. of respiration (Christensen and Pauly, potential impacts of fish production Martinez (1994) found that scale-de- 1993). The peak in transfer efficiency (Carvalho et al., 2010). Comparative pendent food-web structure only pre- at level 3 is due to the consumption analysis of trophic structure in four dicts properties of new, high-quality of high-quality food by carnivores temperate estuaries was conducted in food webs successfully, when more (Manickchand-Heileman et al., 1998). Europe and South Africa. The Finn than 54 species are present. Trophic structure is determined by (1980) cycling index and the whole The Connectance Index and the competitive and predator-prey inter- system average path length were number of possible links in the food actions. It is trophic structure that con- shown to be highest in the most pol- web can be used to assess the matu- trols the fraction of energy consumed luted estuaries (Baird and Ulanowicz, rity of the ecosystem (Manickchand- at each trophic level, rather than being 1993). Heilman et al., 2004). Another de- energy that controls trophic structure Biological metrics for environmental scriptor system is path length, which (Hairston and Hairston 1993). monitoring show a faster and more is the average number of groups that sensitive response to changes in the a flow passes through (Finn, 1980). Anthropic effects quality of benthic environment and Path length also increases with ma- ultimately of the water column (Edgar turity (Christensen and Pauly, 1993). Human interventions or natural distur- et al., 2005). Average fisheries oper- Competition may be a third useful bances can draw a system away from ate around two trophic levels above indicator of the state and health of an the state of maximal complexity. Con- the primary producers (Christensen,

148 Volume 6 number 3  september - december 2011 An overview of studies on trophic ecology in the marine environment: Achievements and perspectives

1996). Fisheries tend to switch from For example, multiple co-occuring verse parasite fauna (Hudson et al., species with high trophic levels to parasites can show different feeding 2006). Parasites have a prominent role species with low trophic levels in strategies and thus lead to complex in ecological networks and may sub- response to changes of their relative and cryptic trophic relationships. This stantially alter food-web structure and abundances (Pauly et al., 2000). complexity and dimensionality of functioning (Amundsen et al., 2009). Humans have historically tended to host-parasite interaction networks is Incoporating parasites into food webs impact higher trophic levels through difficult to disentangle (Gómez-Díaz should become the standard proce- overfishing and hunting of shellfish and González-Solís, 2010). Further- dure in the future (Byers, 2009). In and large coastal marine invertebrates, more, parasites are small and invis- food web studies the key feature is with associated cascading trophic and ible, hidden inside their hosts, and now to understand the complex inter- non-trophic effects. Trophic cascades tend to remain unnoticed unless you actions among hosts, parasites, preda- result in inverse patterns in abun- actively seek them out with the neces- tors and prey. Unraveling the relation- dance or biomass across more than sary expertise. Advances in molecular ship between food web complexity one trophic link in a food web (Car- genetics are now helping to increase and ecosystem stability is becoming penter and Kitchell, 1993). Alterna- the taxonomic resolution of food increasingly important in a world of tive predatory regimes can thus instill webs. For example, DNA barcoding biodiversity loss, and powerfull organization forces in the is aiding in the automated identifica- climate change (Wood, 2007). Para- marine zone (Pace et al., 1999). How- tion of possibly every parasite species sites are far from randomly distributed ever, trophic cascades and top-down within one isolated host (Besansky et in relation to the underlying predator- community regulation as envisioned al., 2003). prey food web (Chen et al., 2008). by trophic-level theories are now re- Parasites have been demonstrated to For example, a prey and its predator garded as relatively uncommon in na- strongly affect food web structure, are more likely to be hosts to the same ture (Polis and Strong, 1996). parasite links being necessary for parasite species (Warren et al., 2010). Feeding relationships and other direct measuring ecosystem stability (Laf- Poulin and Leung (2011) found that and indirect effects need to be taken into ferty et al., 2006). In the first place, small fish are more vulnerable to pre- account when considering the effects the inclusion of parasites and patho- dation, and thus make better hosts for of species loss (Jackson et al., 2001). gens significantly increases the diver- larval parasites. Trophic structure of macrobenthic as- sity of species in food webs (Dobson Given how central food webs are to semblages are closely linked to envi- et al., 2006). There is accumulating fundamental ecological concepts such ronmental characteristics and serve as evidence that parasites have the ca- as stability, diversity and complex- indicators of environmental conditions pacity to affect food-web topology, ity of ecosystems (Pascual and Dune, (Gaston and Nasci, 1988) and for the increasing chain length, connectance 2006), it is important to understand the assessment of anthropic perturbations in and rubustness, as well as stabil- influence of parasites on the structure, marine and estuarine ecosystems (Gray, ity, interaction strength and energy dynamics and function of food webs. 1974; Gaston et al., 1998; Lucero et al., flow (Margogliese, 2002; Lafferty et Because parasites augment the flow 2006). Cardoso et al. (2004) have used al., 2006, 2008; Warren et al., 2010). of energy, alter the strength of interac- macrobenthos feeding guilds distribu- These results show that food webs are tions, change and cause tion to assess impacts. very incomplete without parasites. trophic cascades, the inclusion of in- A variety of theoretical studies sug- fectious agents in food web studies Parasites in food gest that parasites have properties that might permit a better understanding, webs: the penultimate will allow them to play major roles in evaluation and mitigation of human frontier stabilizing the long-term dynamics of impacts on ecosystems, including bi- food webs (Dobson et al., 2006). Par- doversity loss, climate change, exotic is the most common ani- asite species composition may change species, pollution, bioremediation, mal lyfestyle among organisms. Not- in heavily exploited areas (Mar- pest control and fishery exploitation withstanding, attempts to incorporate cogliese, 2002), while keystone para- (Lafferty et al., 2008). Marcogliese parasites and hyperparasites (para- sites will affect important predator or (2002) found that parasite species sites of parasites) into food webs are prey species (Minchella and Scott, composition changes in heavily ex- recent (Huxham and Raffaelli., 1995; 1991). Food-webs contain many more ploited areas to reflect modifications Marcogliese and Cone, 1997; Holt host-parasite links than predator-prey in fish and invertebrate communities. and Hochberg, 1998). This neglect links (Lafferty et al., 2006). Biodiver- Integrating parasites into food webs of parasites is due to the difficulty of sity and production are thus enhanced even changes the paradigmatic view quantifying them by standard ecologi- by parasites, and healthy ecosystems of ecosystems, because top predators cal methods (Lafferty et al., 2005). or food webs should thus have a di- are conceivably no longer the high-

Neotropical Biology and Conservation 149 Martin Lindsey Christoffersen, Maria Elisabeth de Araújo, Joaquim Olinto Branco

est trophic level, as few species com- of the genetic signature of both eco- Mexico based on by-catch. Fisheries Re- pletely lack parasites (Lafferty et al., logical (e.g., filtering) and evolutionary search, 87:46-57. http://dx.doi.org/10.1016/j. 2006). According to Kevin Lafferty, processes (e.g., diversification). fishres.2007.06.019 ADITE, A.; WINEMILLER, K.O. 1997. Troph- “food-web theory is now the frame- Phylogenetic methods predict ecosys- ic ecology and ecomorphology of fish assem- work for modern ecology. Parasites tem function on the basis of related- blages in coastal lakes of Benin, West Africa. have been missing from this frame- ness. For example, plant community Ecoscience, 4:6-23. work, and as a result, we know rela- biomass was found to be better pre- ALBERTONI, E.F.; PALMA-SILVA, C; ES- dicted when considering species relat- TEVES, F.D. 2003. Natural diet of three spe- tively little about the role of parasites cies of shrimp in a tropical coastal lagoon. in ecosystems. It´s like driving with a edness of the community than by tra- Brazilian Archives of Biology and Technology, highway map, but with no knowledge ditional biodiversity indicators such 46:395-403. http://dx.doi.org/10.1590/S1516- of the smaller road network. To reach as number of species or functional 89132003000300011 most destinations, you need a map groups (Cadotte et al., 2008). ALLEN, D.M.; JOHNSON, W.S.; OGBURN Phylogenetic relatedness can also act MATTHEWS, V. 1995. Trophic relation- with both” (Maender, 2006). ships and seasonal utilization of salt-marsh effectively as a proxy for species´ re- creeks by zooplanktivorous fishes. Environ- Further Perspectives sponses to disturbance, and thus these mental Biology of Fishes, 42:37-50. Avail- methods can be applied to temporal able at: https://springerlink3.metapress. Ecosystems evolve through time, slices in order to detect changes in com/content/m2354235843j4005/resource- secured/?target=fulltext.pdf&sid=js2cjijemuf4 since the living world is the product of phylogenetic structure (Helmus et al., utuh2sr5rwnr&sh=www.springerlink.com. Ac- evolution (Gould, 1980). Whichever 2010). Integrating phylogenetics and cess on: 2011/04/22. variables are chosen for study of eco- ecosystem function opens up the pos- AMUNDSEN, P.A.; LAFFERTY, K.D.; KNUD- logical interactions, it is important to sibility of predicting ecological con- SEN, R.; PRIMICERIO, R.; KLEMETSEN, place them in an evolutionary context, sequences of biodiversity shifts in a A.; KURIS, A.M. 2009. Food web topology and parasites in the pelagic zone of a subarctic relating them to their historical devel- changing world. lake. Journal of Animal Ecology, 78:563-572. opment. Since the pioneering effort of Phylogenetics may help to guide better Available at: http://onlinelibrary.wiley.com/ Brooks and McLennan (1991) to inte- taxon sampling of key traits for scal- doi/10.1111/j.1365-2656.2008.01518.x/abstra grate ecology and behavior with phy- ing from organism to global processes ct;jsessionid=195E14986581B99C3B7E7026 logenetics, the importance of studying (Edwards et al., 2007). Phylogenet- 66E61348.d02t01?systemMessage=Wiley+O nline+Library+will+be+disrupted+2+July+fr ecology in a phylogenetic context has ics clearly represents the next break- om+10-12+BST+for+monthly+maintenance. been gradually increasing. through for studies of trophic ecology. Access on: 2011/28/06. However, this perspective is still rare ANGERMEIER, P.L.; WINSTON, M.R. 1998. in trophic studies. The way communi- Acknowledgements Local vs. regional influences on local diversity ties are assembled is an old ecologi- in stream fish communities of Virginia. Ecolo- gy, 79:911-927. http://dx.doi.org/10.1890/0012- cal subject currently experiencing re- The authors thank an anonymous ref- 9658(1998)079[0911:LVRIOL]2.0.CO;2 newed interest thanks to the recent eree (who likens food webs without ARREGUÍN-SÁNCHEZ, F.; VALERO-PA- advances in molecular biology and parasites to physics in a vacuum and CHECO, E.; CHÁVEZ, E.A. 1993. A trophic phylogenetics (Pausas and Verdú, without friction) for instigating us box model of the coastal fish communities of 2010). Webb et al. (2002) provided a to include a whole section on para- the southwestern Gulf of Mexico. In: V. CHRIS- TENSEN; D. PAULY (eds.), Trophic models of novel framework in which phyloge- sites. Luana Poliseli Ramos, Sybelle aquatic ecosystems. Manilla, ICLARM Confer- netic information from co-occuring Bellay and Emmanoela Ferreira are ence Proceedings, p. 197-205. species is used as an indicator of the thanked for providing some papers on BAIRD, D.; ULANOWICZ, R.E. 1993. Com- two main assembly processes of eco- parasites; none of the 2 textbooks pro- parative-study on the trophic structure, cycling logical communities (competition and vided by the latter incorporated para- and ecosystem properties of four tidal estuar- ies. Marine Ecology-Progress Series, 99:221- habitat filtering). sites into food webs as recommended 237. Available at: http://www.int-res.com/ The incorporation of phylogenetics to in the parasite section of this review. articles/meps/99/m099p221.pdf. Access on: the classical approaches has laid the We also thank the productivity grants 2011/04/22. foundation of the emerging research from Conselho Nacional de Desen- BALTZ, D.M.; JONES, R.F. 2003. Temporal volvimento Científico e Tecnológico. and spatial patterns of microhabitat use by fishes area of community phylogenetics. and decapod crustaceans in a Louisiana estuary. Many tools are being developed for de- Transactions of the American Fisheries Society, tecting the underlying forces structur- References 132:662-678. http://dx.doi.org/10.1577/T00-175 ing communities (Cavender-Bares et BASCOMPTE, J. 2009. Disentangling the web al., 2009; Vamosi et al., 2009). Phylo- ABARCA-ARENAS, L.G.; FRANCO-LOPEZ, of life. Science, 325:416-419. Available at: J.; PETERSON, M.S.; BROWN-PETERSON, http://ieg.ebd.csic.es/JordiBascompte/Publica- genetic information will permit a better N.J.; VALERO-PACHECO, E. 2007. So- tions/Science_09.pdf. Access on: 2011/04/22. understanding not only of the historical ciometric analysis of the role of penaeids in BELAN, T.A. 2003. Benthos abundance pat- relationships between species, but also the continental shelf food web off Veracruz, tern and species composition in conditions of

150 Volume 6 number 3  september - december 2011 An overview of studies on trophic ecology in the marine environment: Achievements and perspectives

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