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Gammarus-Microbial Interactions: A Review

Gammarus-Microbial Interactions: A Review Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 295026, 6 pages doi:10.1155/2011/295026 Review Article Daniel Nelson Aquatic Biology Program, Department of Biological Sciences, The University of Alabama, 1106 Bevill Building, 201 Seventh Avenue, P.O. Box 870206, Tuscaloosa, AL 35487, USA Correspondence should be addressed to Daniel Nelson, dnelson12@crimson.ua.edu Received 14 March 2011; Revised 4 May 2011; Accepted 19 May 2011 Academic Editor: Almut Gerhardt Copyright © 2011 Daniel Nelson. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Gammarus spp. are typically classified as shredders under the functional feeding group classification. In the wild and in the laboratory, Gammarus spp. will often shred leaves, breaking them down into finer organic matter fractions. However, leaf litter is a poor quality food source (i.e., high C : N and C : P ratios) and very little leaf material is assimilated by shredders. In freshwater habitats leaf litter is colonized rapidly (within ∼1-2 weeks) by aquatic fungi and bacteria, making the leaves more palatable and nutritious to consumers. Several studies have shown that Gammarus spp. show preference for conditioned leaves over nonconditioned leaves and certain fungal species to others. Furthermore, Gammarus spp. show increased survival and growth rates when fed conditioned leaves compared to non-conditioned leaves. Thus, Gammarus spp. appear to rely on the microbial biofilm associated with leaf detritus as a source of carbon and/or essential nutrients. Also, Gammarus spp. can have both positive and negative effects on the microbial communities on which they fed, making them an important component of the microbial loop in aquatic ecosystems. 1. Introduction ecosystems [15]. Detritus-associated bacteria and fungi are responsible for detrital decomposition and its increase in The diets of amphipods in the genus Gammarus are variable palatability and nutritional quality to consumers [11, 16, 17]. Invertebrate consumers often rely on the microbial biofilm [1]. For example, Gammarus spp. can serve as detritivores [2, 3], herbivores [4, 5], predators [6, 7], and even can- as a carbon source rather than on the detritus itself [11, 14, nibals [2, 8, 9] in aquatic ecosystems. However, under the 18]. Cummins [2] refers to CPOM as a “cracker” and its associated microbes as “peanut butter.” The CPOM (cracker) functional feeding group classification [10–12], Gammarus spp. are typically classified as shredders/facultative shredder acts as a vessel, enabling the consumer to more easily ingest collectors [1]. In the wild and in the laboratory, Gammarus the more nutritious bacteria and fungi (peanut butter). spp. often function as shredders consuming leaves and other Over the years, research has shown that Gammarus coarse particulate organic matter (CPOM), breaking it down spp. feed on conditioned or inoculated detritus (i.e., leaves, into smaller fractions or fine particulate organic matter leaf discs, or sediment) with “suitable” microflora [17, 19– (FPOM). Microbes, such as bacteria and fungi, are often 22]. In addition, research has shown higher survival and associated with particulate organic matter such as leaves growth rates of Gammarus amphipods in the laboratory and decaying wood [13, 14]. Leaf detritus, in particular, when theyare fedleaveswithfungalgrowthcomparedto is an important carbon source for the microbial loop in unconditioned or sterile leaves [20, 23, 24]. Freshly shed aquatic ecosystems [13]. Leaf matter serves as a substrate and sterile leaves typically have low nutritive value (i.e., for bacterial and fungal growth, while at the same time high C:N and C : P ratios) and contain high amounts of supplying the microbial community with carbon in the lignin and cellulose, which are virtually indigestible to most form of leached dissolved organic carbon (DOC) [13]. invertebrates [25]. Therefore, for shredders, the percentage Along with physical abrasion and soluble organic matter of food ingested and converted into invertebrate biomass is leaching, microbial decomposition and invertebrate feeding typically very low. As a result, many shredders, including interact to regulate leaf litter breakdown rate in aquatic Gammarus amphipods, wait until microbes (which are 2 International Journal of Zoology typically highly nutritious) colonize and build up on this troglophilus ingested the elm leaves and ignored the oak. poorly nutritious food before feeding. Pockl ¨ [23] simultaneously offered G. fossarum and G. roeseli Gammarus spp. have also been shown to have both eight different naturally decaying (i.e., conditioned) leaf negative and positive effects on the microbial communities species. The most preferred and quickly eaten were leaf discs on which they feed, illustrating the importance of this genus of lime, ash, and alder. Both species showed little interest to the microbial loop in lotic and lentic ecosystems. Most in oak leaves, and beech leaf discs were nearly untouched research investigating interactions between microbes and [23]. This behavior most likely resulted from differences invertebrates has been focused on the role of microbes as a in toughness of the leaves, leaf thickness, and chemical potential food source [26]. Although relatively little is known constituents (e.g., phenols and tannins) [23]. of the feedback effects that grazing invertebrates, such as To determine if G. minus could distinguish different Gammarus amphipods, can have on their microbial food foods and exhibit a preference for the different foods, Kosta- [26], it has been demonstrated that microbial metabolism, los and Seymour [20]performed aseriesoflaboratoryand production, and biomass can be influenced by both “bottom- field experiments. They individually compared preference up” and “top-down” controls [27–29]. Although invertebrate of five different foods against a control, which contained a feeding can decrease microbial biofilm biomass, it has also microflora most similar to fresh stream leaves [20]. The five been shown to stimulate microbial growth and activity [27, different foods consisted of elm leaves with no microflora 30]. Thus, Gammarus spp. are often involved in a feedback (sterile), bacteria-enriched elm leaves, conditioned elm loop with the microbial community on which they feed. In leaves with a reduced bacterial fauna (still containing fungi), some cases, these feedbacks can be positive [28–30], while in fungus-enriched (Tetrachaetum elegans) elm leaves, and the others, they can be negative [29]. fungus T. elegans alone. Gammarus minus most strongly Thespecific objectiveofthisreviewistoevaluatewhat preferred the fungus-enriched leaves and conditioned leaves is known regarding how microbes influence Gammarus spp. with a reduced bacterial fauna to the control leaves. The feeding preference, survival, and growth in the laboratory sterile elm leaves were least preferred. and aquatic habitats. In addition, it will be discussed In another laboratory study, Friberg and Jacobsen [41] how Gammarus spp. affect the microbial community on examined the feeding preferences of G. pulex.Overall, G. which they feed, either through ingestion or other types of pulex preferred conditioned alder leaves over five other food interactions. Finally, the current state of research investigat- items which included conditioned beech leaves, fresh beech ing Gammarus-microbial interactions will be reviewed and leaves, Sitka spruce needles, a fresh macrophyte, and a possible future research directions will be discussed. fresh filamentous green algae. The authors found no linear relationships between food preference and fiber content, toughness, phosphorous content, nitrogen content, and C:N 2. Food Selection, Survival, and Growth ratio, leading them to believe that bacterial or fungal coating Quality of detritus is an important factor that determines was responsible for the preference patterns. In another study food selection by shredders. Research has shown that using G. pulex,Grac¸a et al. [42] demonstrated that when shredders tend to prefer certain leaf species to others [31– offered a choice between unconditioned leaf discs of elm, leaf discs of elm inoculated with the fungus Anguillospora 33] and conditioned leaves over non-conditioned leaves [33–40]. Typically, shredders select food based on several longissima,or A. longissima mycelia, G. pulex wasableto characteristics of leaves, which include toughness, nutrient discriminate between the different foods and concentrated its feeding on the inoculated leaf discs, and to a lesser content, and the degree of conditioning by microbes [40]. Gammarus spp. are no exception [19, 20, 23, 31, 33, 41]. extent, on the unconditioned leaf discs. The A. longissima In some of the earliest laboratory experiments investigating mycelia were ignored by G. pulex. Because food preference food selection by Gammarus spp., Barloc ¨ her and Kendrick was not correlated with fungal biomass, leaf disc toughness, [19] investigated food (leaf species) and fungi preference leaf decomposition, or nitrogen content, Grac¸a et al. [42] of Gammarus pseudolimnaeus. When very little microflora concluded that other unmeasured factors could have affected were present on leaf discs, G. pseudolimnaeus preferred ash to food preference by G. pulex. These could include the fungal maple and maple to oak leaves. Barloc ¨ her and Kendrick [19] synthesis of micronutrients or the differential ability of fungi to eliminate plant allelochemicals among others [42]. then presented amphipods with pure colonies of ten different hyphomycetes along with maple leaf discs with very little Gammarus spp. have also been shown to prefer particular associated microflora. Gammarus pseudolimnaeus always fungal species to others. When offered leaves colonized separately by one of eight species of aquatic hyphomycetes, preferred the fungus to the leaf discs and in several cases the amphipods entirely ignored the leaves and consumed only Arsuffi and Suberkropp [17]found Gammarus amphipods the hyphomycetes. to be highly selective feeders. Leaves colonized by the As Barloc ¨ her and Kendrick [19]demonstrated, G. pseu- fungus Alatospora acuminata were the most preferred, but dolimnaeus can exhibit preference for certain conditioned Gammarus also fed on leaves colonized by Clavariopsis aquatica and Flagellospora curvula. Feeding on other aquatic leaf species over others. Other Gammarus spp. have shown similar preferences. In the laboratory, the stygophilic G. hyphomycetes was negligible [17]. Aquatic hyphomycetes troglophilus consumed conditioned oak if they were the produce secondary metabolites that function in microbe- microbe interactions and may also defend the fungi from only leaves presented to it [31]. However, if presented with conditioned oak and elm leaves simultaneously, G. invertebrate feeding. Arsuffi andSuberkropp[17]suggest International Journal of Zoology 3 that secondary metabolites from fungi are responsible for or a reduced microflora [20]. Other Gammarus spp. have the variation observed in feeding preferences, growth rates, shown higher growth rates when fed conditioned leaves. and survivorship of shredders consuming leaves colonized by Grac¸a et al. [33] found that conditioning had a significant different fungi [17]. effect on the growth of G. pulex. Similarly, Pockl ¨ [23]found The combination of leaf and fungal species has also that neonates, juveniles, and early adults of G. fossarum been shown to influence selection by Gammarus spp. In and G. roeseli fed leached and decaying leaves of lime, a laboratory study, individuals of G. tigrinus were given elm, and hornbeam with surface growth of aquatic fungi a choice between six different leaf/fungus combinations and bacteria had higher growth rates than amphipods fed [21]. The leaf discs were conditioned with single species of fresh, growing leaves. These studies suggest that microbes, aquatic hyphomycetes and their concentrations of proteins, particularly fungi, confer an advantage to Gammarus spp. by lipids, and ergosterol (an indicator of fungal biomass) were positively influencing survival, growth rates, or both. measured. Although total consumption was not correlated In contrast, Grac¸a et al. [24] found no significant increase to the lipid or protein content of the leaves or the fungal in the survival of G. pulex on fungally conditioned leaf biomass, G. tigrinus showed a slight preference for some material when compared to unconditioned food. In general, leaf/fungal combinations over others [21]. The authors survival of G. pulex was low on both conditioned and uncon- then extracted fungal mycelia and applied the extracts ditioned leaves [24]. Although growth rates were higher on to unconditioned leaf discs. Gammarus tigrinus preferred conditioned leaf material, the difference was not significant naturally conditioned leaf discs to the extract-coated leaf [24]. The authors offered an explanation for this lack of discs, suggesting that natural colonization over time makes significance, using the results of an energy budget study. the leaf/fungi combination more attractive compared to a Individuals of G. pulex feeding on unconditioned leaves had rapid assembly of the parts. a significantly lower respiration rate than those individuals In a more recent study, Assmann and Elert [22] exam- feeding on conditioned leaves. The authors hypothesized that ined the role of fungal attractants and repellents in food pref- the lower metabolic demands as a result of a lower respiration erence of the amphipod G. roeseli. Because both attractants rate compensated for the reduced energy intake. Thus, G. and repellents seemed to act on G. roeseli feeding preference, pulex is able to maintain a constant growth rate, even when the authors suggest that the relative ratios of repellents food quality is poor. and attractants might determine consumption of fungi by Gammarus. Furthermore, changes in the environment could 3. Effects of Feeding on lead to changes in the relative ratio of attractants to repellents the Microbial Community [22]. Thus, food preference may be governed by environ- mental conditions rather than being fixed in the consumer. The effect Gammarus spp. have on microbial communi- Amphipods fed conditioned leaves and/or fungi have ties is not well known. Obviously, Gammarus amphipods increased assimilation efficiencies. Low assimilation effi- can influence microbial biomass and production through ciency results in less matter and energy available for main- mechanical removal (i.e., direct consumption). Direct con- tenance, growth, and reproduction [43], thus compromising sumption of biofilms by invertebrates has been shown to performance. Barloc ¨ her and Kendrick [44] compared the decrease microbial biomass and alter microbial community assimilation efficiencies of G. pseudolimnaeus fed elm leaves, composition [45–49], however, consumption has also been maple leaves, or the mycelium of one of ten fungi (5 aquatic shown to stimulate microbial growth [27, 30]. Shredding of hyphomycetes and 5 terrestrial hyphomycetes). Although the leaves by Gammarus spp. may enhance microbial respiration amount of food consumed was ten times greater in all of by increasing the surface area of the leaf, which can lead the leaf diets than in the fungi diets, the highest assimilation to higher microbial respiration per unit mass of leaves efficiencies were found for those individuals fed four of the [30]. In addition, increased fragmentation of leaves and ten fungi. Only 10% of the dry mass, 14–18% of the protein, excretion by Gammarus amphipods may lead to an increase and 17–19% of the energy of either elm or maple leaves were in the availability of DOC and inorganic nutrients [30]. assimilated by the amphipods. However, G. pseudolimnaeus Thus, if a biofilm is nutrient limited, leaf shredding by assimilated approximately 43–76% of the dry mass, 73–96% Gammarus spp. can possibly relieve nutrient limitation of the protein, and 70–83% of the energy when fed fungal constraints. Direct consumption by Gammarus spp. can mycelium commonly found in streams [44]. not only directly decrease microbial biomass, but it can Research has shown higher survival and growth rates also change biofilm architecture, thus altering the delivery when Gammarus spp. are fed conditioned leaves compared of inorganic nutrients and energy to the biofilm [29, 49]. to non-conditioned or sterile leaves. In addition to their Morrison and White [27] showed that microbial biomass experiments on food preference, Kostalos and Seymour was higher on detritus (conditioned oak leaves) that had [20] experimentally tested the survival of G. minus on been grazed by G. mucronatus than on ungrazed detritus. ten different diets. These experiments showed significant In addition to increasing microbial biomass, grazing by differences in survivorship over a ten-week period, with G. mucronatus increased metabolic activity and changed the highest survivorship (45–88%) occurring on fungus- microbial community structure [27]. As amphipods grazed, enriched leaves [20]. Intermediate survival rates (36–63%) microbial community structure shifted from one with both occurred on leaves with a viable bacterial flora while the prokaryotes (bacteria) and microeukaryotes (fungi) to one lowest survivorship (∼3%) occurred on leaves that had no dominated by bacteria [27]. Because microbial biofilms are 4 International Journal of Zoology important mediators of energy flux and nutrient transfor- imbalances between detritivores (e.g., shredders) and their mation in aquatic habitats, changes in microbial biomass, food canbecommon[53, 56–58]. An inadequate supply of community composition, and biofilm architecture may have one or more nutrients can constrain animal growth and alter profound effects on aquatic ecosystem functioning [50, 51]. their life history [57]. One way in which to examine the More recently, Kinsey et al. [30] compared the influence nutrient deficiency in consumers is the threshold elemental of feeding by cave and surface forms of G. minus on microbial ratio (TER). Threshold elemental ratios are elemental ratios biofilms and found that both forms increased the respiration at which growth limitation of a consumer switches from one rate of leaf-associated microbes by 32–52%. However, the element to another [52, 57]. Calculation of TERs (C:N and cave form had a 15% greater stimulatory effect on microbial C : P) requires estimates of assimilation efficiencies for C, respiration. Kinsey et al. [30] concluded that their results N, and P, ingestion rates, respiration rates, and %C, %N, may have been due to an attraction of G. minus to leaves and %P of consumers. When the TER of the consumer is with greater microbial growth or due to the amphipods stim- equal to the C:nutrient ratio of the consumer’s food, animal ulating microbial respiration by (1) increasing the availability growth is limited by both C and the nutrient [53]. When the of DOM and inorganic nutrients through fragmentation TER of the consumer deviates from the C:nutrient ratio of and excretion, (2) increasing water flow over the microbial the food, either C or the nutrient is limiting [53]. Further biofilm, thus reducing boundary layer effects and increasing elucidation of the importance of highly nutritious microbes diffusion rates of nutrients and oxygen into biofilms, or in Gammarus diets could be provided by identifying the (3) increasing leaf surface area, thereby increasing microbial critical C:N or C : P ratios of detritus and microbes and the respiration per unit mass of leaves. Cooney and Simon [29] TERs of Gammarus spp. then used microcosm experiments to examine how bacterial Fatty acids (e.g., polyunsaturated fatty acids (PUFAs) production on rocks and fine sediments from cave streams and highly unsaturated fatty acids (HUFAs)) are critical responded to amendments of dissolved organic matter biological compounds in aquatic food webs [58, 59]. Some (DOM) and to the cave form of G. minus. Interestingly, fatty acids are critical for growth and reproduction while feeding by G. minus strongly suppressed bacterial production others are thought to maintain membrane fluidity at low on rocks but had no effect on bacterial production on temperatures [59]. However, little is known about the fatty fine sediments. In addition, microbial production on rocks acid requirements for Gammarus spp. in lakes and streams. was stimulated by DOM amendments but production on Gammarus spp., like other invertebrates, have fatty acid sediments was not. Their results indicate that both resources requirements that must be filled through their diet as and consumers play important roles in regulating microbial evidence for synthesis de novo has not been found. Future activity, particularly on rocky substrates. research should address the trophic transfer of essential fatty acids from microbes to Gammarus amphipods, as this research could make important contributions to Gammarus- 4. Conclusions microbe food web ecology and to our understanding of the This paper illustrates the importance of bacteria and fungi microbial loop. in the diet of Gammarus amphipods. It has been shown that Gammarus spp. frequently prefer certain leaf species Acknowledgments to others and conditioned leaves to unconditioned leaves. Conditioning of detritus often enhances survival and even The author wishes to thank Frank M. Wilhelm and Chau growth of Gammarus amphipods. Furthermore, Gammarus D. Tran for insightful comments on an earlier version of can have a significant influence on microbial communities this paper. In addition, this paper was greatly improved by through consumption of microbially enriched detritus, par- comments from an anonymous reviewer. ticularly fallen leaves. Although there is a body of literature on the interactions between Gammarus spp. and microbes, References the full story is not complete. 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Gammarus-Microbial Interactions: A Review

International Journal of Zoology , Volume 2011 – Jul 20, 2011

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Copyright © 2011 Daniel Nelson. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Publishing Corporation International Journal of Zoology Volume 2011, Article ID 295026, 6 pages doi:10.1155/2011/295026 Review Article Daniel Nelson Aquatic Biology Program, Department of Biological Sciences, The University of Alabama, 1106 Bevill Building, 201 Seventh Avenue, P.O. Box 870206, Tuscaloosa, AL 35487, USA Correspondence should be addressed to Daniel Nelson, dnelson12@crimson.ua.edu Received 14 March 2011; Revised 4 May 2011; Accepted 19 May 2011 Academic Editor: Almut Gerhardt Copyright © 2011 Daniel Nelson. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Gammarus spp. are typically classified as shredders under the functional feeding group classification. In the wild and in the laboratory, Gammarus spp. will often shred leaves, breaking them down into finer organic matter fractions. However, leaf litter is a poor quality food source (i.e., high C : N and C : P ratios) and very little leaf material is assimilated by shredders. In freshwater habitats leaf litter is colonized rapidly (within ∼1-2 weeks) by aquatic fungi and bacteria, making the leaves more palatable and nutritious to consumers. Several studies have shown that Gammarus spp. show preference for conditioned leaves over nonconditioned leaves and certain fungal species to others. Furthermore, Gammarus spp. show increased survival and growth rates when fed conditioned leaves compared to non-conditioned leaves. Thus, Gammarus spp. appear to rely on the microbial biofilm associated with leaf detritus as a source of carbon and/or essential nutrients. Also, Gammarus spp. can have both positive and negative effects on the microbial communities on which they fed, making them an important component of the microbial loop in aquatic ecosystems. 1. Introduction ecosystems [15]. Detritus-associated bacteria and fungi are responsible for detrital decomposition and its increase in The diets of amphipods in the genus Gammarus are variable palatability and nutritional quality to consumers [11, 16, 17]. Invertebrate consumers often rely on the microbial biofilm [1]. For example, Gammarus spp. can serve as detritivores [2, 3], herbivores [4, 5], predators [6, 7], and even can- as a carbon source rather than on the detritus itself [11, 14, nibals [2, 8, 9] in aquatic ecosystems. However, under the 18]. Cummins [2] refers to CPOM as a “cracker” and its associated microbes as “peanut butter.” The CPOM (cracker) functional feeding group classification [10–12], Gammarus spp. are typically classified as shredders/facultative shredder acts as a vessel, enabling the consumer to more easily ingest collectors [1]. In the wild and in the laboratory, Gammarus the more nutritious bacteria and fungi (peanut butter). spp. often function as shredders consuming leaves and other Over the years, research has shown that Gammarus coarse particulate organic matter (CPOM), breaking it down spp. feed on conditioned or inoculated detritus (i.e., leaves, into smaller fractions or fine particulate organic matter leaf discs, or sediment) with “suitable” microflora [17, 19– (FPOM). Microbes, such as bacteria and fungi, are often 22]. In addition, research has shown higher survival and associated with particulate organic matter such as leaves growth rates of Gammarus amphipods in the laboratory and decaying wood [13, 14]. Leaf detritus, in particular, when theyare fedleaveswithfungalgrowthcomparedto is an important carbon source for the microbial loop in unconditioned or sterile leaves [20, 23, 24]. Freshly shed aquatic ecosystems [13]. Leaf matter serves as a substrate and sterile leaves typically have low nutritive value (i.e., for bacterial and fungal growth, while at the same time high C:N and C : P ratios) and contain high amounts of supplying the microbial community with carbon in the lignin and cellulose, which are virtually indigestible to most form of leached dissolved organic carbon (DOC) [13]. invertebrates [25]. Therefore, for shredders, the percentage Along with physical abrasion and soluble organic matter of food ingested and converted into invertebrate biomass is leaching, microbial decomposition and invertebrate feeding typically very low. As a result, many shredders, including interact to regulate leaf litter breakdown rate in aquatic Gammarus amphipods, wait until microbes (which are 2 International Journal of Zoology typically highly nutritious) colonize and build up on this troglophilus ingested the elm leaves and ignored the oak. poorly nutritious food before feeding. Pockl ¨ [23] simultaneously offered G. fossarum and G. roeseli Gammarus spp. have also been shown to have both eight different naturally decaying (i.e., conditioned) leaf negative and positive effects on the microbial communities species. The most preferred and quickly eaten were leaf discs on which they feed, illustrating the importance of this genus of lime, ash, and alder. Both species showed little interest to the microbial loop in lotic and lentic ecosystems. Most in oak leaves, and beech leaf discs were nearly untouched research investigating interactions between microbes and [23]. This behavior most likely resulted from differences invertebrates has been focused on the role of microbes as a in toughness of the leaves, leaf thickness, and chemical potential food source [26]. Although relatively little is known constituents (e.g., phenols and tannins) [23]. of the feedback effects that grazing invertebrates, such as To determine if G. minus could distinguish different Gammarus amphipods, can have on their microbial food foods and exhibit a preference for the different foods, Kosta- [26], it has been demonstrated that microbial metabolism, los and Seymour [20]performed aseriesoflaboratoryand production, and biomass can be influenced by both “bottom- field experiments. They individually compared preference up” and “top-down” controls [27–29]. Although invertebrate of five different foods against a control, which contained a feeding can decrease microbial biofilm biomass, it has also microflora most similar to fresh stream leaves [20]. The five been shown to stimulate microbial growth and activity [27, different foods consisted of elm leaves with no microflora 30]. Thus, Gammarus spp. are often involved in a feedback (sterile), bacteria-enriched elm leaves, conditioned elm loop with the microbial community on which they feed. In leaves with a reduced bacterial fauna (still containing fungi), some cases, these feedbacks can be positive [28–30], while in fungus-enriched (Tetrachaetum elegans) elm leaves, and the others, they can be negative [29]. fungus T. elegans alone. Gammarus minus most strongly Thespecific objectiveofthisreviewistoevaluatewhat preferred the fungus-enriched leaves and conditioned leaves is known regarding how microbes influence Gammarus spp. with a reduced bacterial fauna to the control leaves. The feeding preference, survival, and growth in the laboratory sterile elm leaves were least preferred. and aquatic habitats. In addition, it will be discussed In another laboratory study, Friberg and Jacobsen [41] how Gammarus spp. affect the microbial community on examined the feeding preferences of G. pulex.Overall, G. which they feed, either through ingestion or other types of pulex preferred conditioned alder leaves over five other food interactions. Finally, the current state of research investigat- items which included conditioned beech leaves, fresh beech ing Gammarus-microbial interactions will be reviewed and leaves, Sitka spruce needles, a fresh macrophyte, and a possible future research directions will be discussed. fresh filamentous green algae. The authors found no linear relationships between food preference and fiber content, toughness, phosphorous content, nitrogen content, and C:N 2. Food Selection, Survival, and Growth ratio, leading them to believe that bacterial or fungal coating Quality of detritus is an important factor that determines was responsible for the preference patterns. In another study food selection by shredders. Research has shown that using G. pulex,Grac¸a et al. [42] demonstrated that when shredders tend to prefer certain leaf species to others [31– offered a choice between unconditioned leaf discs of elm, leaf discs of elm inoculated with the fungus Anguillospora 33] and conditioned leaves over non-conditioned leaves [33–40]. Typically, shredders select food based on several longissima,or A. longissima mycelia, G. pulex wasableto characteristics of leaves, which include toughness, nutrient discriminate between the different foods and concentrated its feeding on the inoculated leaf discs, and to a lesser content, and the degree of conditioning by microbes [40]. Gammarus spp. are no exception [19, 20, 23, 31, 33, 41]. extent, on the unconditioned leaf discs. The A. longissima In some of the earliest laboratory experiments investigating mycelia were ignored by G. pulex. Because food preference food selection by Gammarus spp., Barloc ¨ her and Kendrick was not correlated with fungal biomass, leaf disc toughness, [19] investigated food (leaf species) and fungi preference leaf decomposition, or nitrogen content, Grac¸a et al. [42] of Gammarus pseudolimnaeus. When very little microflora concluded that other unmeasured factors could have affected were present on leaf discs, G. pseudolimnaeus preferred ash to food preference by G. pulex. These could include the fungal maple and maple to oak leaves. Barloc ¨ her and Kendrick [19] synthesis of micronutrients or the differential ability of fungi to eliminate plant allelochemicals among others [42]. then presented amphipods with pure colonies of ten different hyphomycetes along with maple leaf discs with very little Gammarus spp. have also been shown to prefer particular associated microflora. Gammarus pseudolimnaeus always fungal species to others. When offered leaves colonized separately by one of eight species of aquatic hyphomycetes, preferred the fungus to the leaf discs and in several cases the amphipods entirely ignored the leaves and consumed only Arsuffi and Suberkropp [17]found Gammarus amphipods the hyphomycetes. to be highly selective feeders. Leaves colonized by the As Barloc ¨ her and Kendrick [19]demonstrated, G. pseu- fungus Alatospora acuminata were the most preferred, but dolimnaeus can exhibit preference for certain conditioned Gammarus also fed on leaves colonized by Clavariopsis aquatica and Flagellospora curvula. Feeding on other aquatic leaf species over others. Other Gammarus spp. have shown similar preferences. In the laboratory, the stygophilic G. hyphomycetes was negligible [17]. Aquatic hyphomycetes troglophilus consumed conditioned oak if they were the produce secondary metabolites that function in microbe- microbe interactions and may also defend the fungi from only leaves presented to it [31]. However, if presented with conditioned oak and elm leaves simultaneously, G. invertebrate feeding. Arsuffi andSuberkropp[17]suggest International Journal of Zoology 3 that secondary metabolites from fungi are responsible for or a reduced microflora [20]. Other Gammarus spp. have the variation observed in feeding preferences, growth rates, shown higher growth rates when fed conditioned leaves. and survivorship of shredders consuming leaves colonized by Grac¸a et al. [33] found that conditioning had a significant different fungi [17]. effect on the growth of G. pulex. Similarly, Pockl ¨ [23]found The combination of leaf and fungal species has also that neonates, juveniles, and early adults of G. fossarum been shown to influence selection by Gammarus spp. In and G. roeseli fed leached and decaying leaves of lime, a laboratory study, individuals of G. tigrinus were given elm, and hornbeam with surface growth of aquatic fungi a choice between six different leaf/fungus combinations and bacteria had higher growth rates than amphipods fed [21]. The leaf discs were conditioned with single species of fresh, growing leaves. These studies suggest that microbes, aquatic hyphomycetes and their concentrations of proteins, particularly fungi, confer an advantage to Gammarus spp. by lipids, and ergosterol (an indicator of fungal biomass) were positively influencing survival, growth rates, or both. measured. Although total consumption was not correlated In contrast, Grac¸a et al. [24] found no significant increase to the lipid or protein content of the leaves or the fungal in the survival of G. pulex on fungally conditioned leaf biomass, G. tigrinus showed a slight preference for some material when compared to unconditioned food. In general, leaf/fungal combinations over others [21]. The authors survival of G. pulex was low on both conditioned and uncon- then extracted fungal mycelia and applied the extracts ditioned leaves [24]. Although growth rates were higher on to unconditioned leaf discs. Gammarus tigrinus preferred conditioned leaf material, the difference was not significant naturally conditioned leaf discs to the extract-coated leaf [24]. The authors offered an explanation for this lack of discs, suggesting that natural colonization over time makes significance, using the results of an energy budget study. the leaf/fungi combination more attractive compared to a Individuals of G. pulex feeding on unconditioned leaves had rapid assembly of the parts. a significantly lower respiration rate than those individuals In a more recent study, Assmann and Elert [22] exam- feeding on conditioned leaves. The authors hypothesized that ined the role of fungal attractants and repellents in food pref- the lower metabolic demands as a result of a lower respiration erence of the amphipod G. roeseli. Because both attractants rate compensated for the reduced energy intake. Thus, G. and repellents seemed to act on G. roeseli feeding preference, pulex is able to maintain a constant growth rate, even when the authors suggest that the relative ratios of repellents food quality is poor. and attractants might determine consumption of fungi by Gammarus. Furthermore, changes in the environment could 3. Effects of Feeding on lead to changes in the relative ratio of attractants to repellents the Microbial Community [22]. Thus, food preference may be governed by environ- mental conditions rather than being fixed in the consumer. The effect Gammarus spp. have on microbial communi- Amphipods fed conditioned leaves and/or fungi have ties is not well known. Obviously, Gammarus amphipods increased assimilation efficiencies. Low assimilation effi- can influence microbial biomass and production through ciency results in less matter and energy available for main- mechanical removal (i.e., direct consumption). Direct con- tenance, growth, and reproduction [43], thus compromising sumption of biofilms by invertebrates has been shown to performance. Barloc ¨ her and Kendrick [44] compared the decrease microbial biomass and alter microbial community assimilation efficiencies of G. pseudolimnaeus fed elm leaves, composition [45–49], however, consumption has also been maple leaves, or the mycelium of one of ten fungi (5 aquatic shown to stimulate microbial growth [27, 30]. Shredding of hyphomycetes and 5 terrestrial hyphomycetes). Although the leaves by Gammarus spp. may enhance microbial respiration amount of food consumed was ten times greater in all of by increasing the surface area of the leaf, which can lead the leaf diets than in the fungi diets, the highest assimilation to higher microbial respiration per unit mass of leaves efficiencies were found for those individuals fed four of the [30]. In addition, increased fragmentation of leaves and ten fungi. Only 10% of the dry mass, 14–18% of the protein, excretion by Gammarus amphipods may lead to an increase and 17–19% of the energy of either elm or maple leaves were in the availability of DOC and inorganic nutrients [30]. assimilated by the amphipods. However, G. pseudolimnaeus Thus, if a biofilm is nutrient limited, leaf shredding by assimilated approximately 43–76% of the dry mass, 73–96% Gammarus spp. can possibly relieve nutrient limitation of the protein, and 70–83% of the energy when fed fungal constraints. Direct consumption by Gammarus spp. can mycelium commonly found in streams [44]. not only directly decrease microbial biomass, but it can Research has shown higher survival and growth rates also change biofilm architecture, thus altering the delivery when Gammarus spp. are fed conditioned leaves compared of inorganic nutrients and energy to the biofilm [29, 49]. to non-conditioned or sterile leaves. In addition to their Morrison and White [27] showed that microbial biomass experiments on food preference, Kostalos and Seymour was higher on detritus (conditioned oak leaves) that had [20] experimentally tested the survival of G. minus on been grazed by G. mucronatus than on ungrazed detritus. ten different diets. These experiments showed significant In addition to increasing microbial biomass, grazing by differences in survivorship over a ten-week period, with G. mucronatus increased metabolic activity and changed the highest survivorship (45–88%) occurring on fungus- microbial community structure [27]. As amphipods grazed, enriched leaves [20]. Intermediate survival rates (36–63%) microbial community structure shifted from one with both occurred on leaves with a viable bacterial flora while the prokaryotes (bacteria) and microeukaryotes (fungi) to one lowest survivorship (∼3%) occurred on leaves that had no dominated by bacteria [27]. Because microbial biofilms are 4 International Journal of Zoology important mediators of energy flux and nutrient transfor- imbalances between detritivores (e.g., shredders) and their mation in aquatic habitats, changes in microbial biomass, food canbecommon[53, 56–58]. An inadequate supply of community composition, and biofilm architecture may have one or more nutrients can constrain animal growth and alter profound effects on aquatic ecosystem functioning [50, 51]. their life history [57]. One way in which to examine the More recently, Kinsey et al. [30] compared the influence nutrient deficiency in consumers is the threshold elemental of feeding by cave and surface forms of G. minus on microbial ratio (TER). Threshold elemental ratios are elemental ratios biofilms and found that both forms increased the respiration at which growth limitation of a consumer switches from one rate of leaf-associated microbes by 32–52%. However, the element to another [52, 57]. Calculation of TERs (C:N and cave form had a 15% greater stimulatory effect on microbial C : P) requires estimates of assimilation efficiencies for C, respiration. Kinsey et al. [30] concluded that their results N, and P, ingestion rates, respiration rates, and %C, %N, may have been due to an attraction of G. minus to leaves and %P of consumers. When the TER of the consumer is with greater microbial growth or due to the amphipods stim- equal to the C:nutrient ratio of the consumer’s food, animal ulating microbial respiration by (1) increasing the availability growth is limited by both C and the nutrient [53]. When the of DOM and inorganic nutrients through fragmentation TER of the consumer deviates from the C:nutrient ratio of and excretion, (2) increasing water flow over the microbial the food, either C or the nutrient is limiting [53]. Further biofilm, thus reducing boundary layer effects and increasing elucidation of the importance of highly nutritious microbes diffusion rates of nutrients and oxygen into biofilms, or in Gammarus diets could be provided by identifying the (3) increasing leaf surface area, thereby increasing microbial critical C:N or C : P ratios of detritus and microbes and the respiration per unit mass of leaves. Cooney and Simon [29] TERs of Gammarus spp. then used microcosm experiments to examine how bacterial Fatty acids (e.g., polyunsaturated fatty acids (PUFAs) production on rocks and fine sediments from cave streams and highly unsaturated fatty acids (HUFAs)) are critical responded to amendments of dissolved organic matter biological compounds in aquatic food webs [58, 59]. Some (DOM) and to the cave form of G. minus. Interestingly, fatty acids are critical for growth and reproduction while feeding by G. minus strongly suppressed bacterial production others are thought to maintain membrane fluidity at low on rocks but had no effect on bacterial production on temperatures [59]. However, little is known about the fatty fine sediments. In addition, microbial production on rocks acid requirements for Gammarus spp. in lakes and streams. was stimulated by DOM amendments but production on Gammarus spp., like other invertebrates, have fatty acid sediments was not. Their results indicate that both resources requirements that must be filled through their diet as and consumers play important roles in regulating microbial evidence for synthesis de novo has not been found. Future activity, particularly on rocky substrates. research should address the trophic transfer of essential fatty acids from microbes to Gammarus amphipods, as this research could make important contributions to Gammarus- 4. Conclusions microbe food web ecology and to our understanding of the This paper illustrates the importance of bacteria and fungi microbial loop. in the diet of Gammarus amphipods. It has been shown that Gammarus spp. frequently prefer certain leaf species Acknowledgments to others and conditioned leaves to unconditioned leaves. Conditioning of detritus often enhances survival and even The author wishes to thank Frank M. Wilhelm and Chau growth of Gammarus amphipods. Furthermore, Gammarus D. Tran for insightful comments on an earlier version of can have a significant influence on microbial communities this paper. In addition, this paper was greatly improved by through consumption of microbially enriched detritus, par- comments from an anonymous reviewer. ticularly fallen leaves. Although there is a body of literature on the interactions between Gammarus spp. and microbes, References the full story is not complete. 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