A review on the effects of antimicrobials use in cultures of planktonic organisms: a procedure for ecological experiments.
INTRODUCTIONPlankton is the term used for all living organisms floating or drifting in the water column that have little or no ability to swim against currents (Haeckel, 1893), including virus (virioplankton), bacteria (bacterioplankton), filamentous fungi and yeasts (mycoplankton), microalgae (phytoplankton) and phagotrofic organisms (zooplankton) (Johnson & Allen, 2012). These organisms, as a whole, play a vital role in the food chain (classical and microbial loop), in some cases as prey and in others as predators (Hopcroft & Roff, 1998), maintaining the balance of aquatic populations and cycling nutrients in this environment (biochemical cycles) (Calbet & Saiz, 2016).
In addition, plankton plays a key role in benthicpelagic coupling, marine snow formation and biological pump (Schnack-Schiel & Isla, 2005; Turner, 2015; Agostini et al., 2018). It can also be used as biological indicators of water masses, ocean currents, pollution and climate changes (Reid & Edwards, 2001; Johnson & Allen, 2012). For this reason, there is great interest in understanding how the processes involving the planktonic community work, and how these organisms intereact with other organisms, being the phytoplankton and zooplankton the groups most studied, usually through the establishment of laboratory cultures.
Laboratory cultivation has been established in order to answer a series of questions about the biology and ecology of these organisms, facilitating genetic, cytology, morphology, physiology, development and taxonomy studies, as well as intra and inter-specific interaction studies (Trottet et al., 2011). Furthermore, planktonic organisms are commonly cultivated intensively for use in the aquaculture sector (Schipp et al., 1999), principally as the live food of commercial species of fish, mollusks and crustaceans (Creswell, 2010). However, when at high densities these cultures result in large loads of waste and organic matter (Olafsen, 1993), favoring the proliferation of virioplankton, mycoplankton and particularly free and/or adhered bacterioplankton, which can benefit or harm the culture, depending on the researcher aim.
Effects of bacteria and fungi in cultures
In aquaculture, for example, the biofloc tec (BFT) system comprises an association (aggregates) of bacteria, phytoplankton, fungi, virus and particulate organic matter, as well as bacterial grazers which benefit shrimp culture (Hargreaves, 2006). These aggregates or biofilms (bacteria systematically arranged in a self-produced polymeric matrix) (Vasudevan, 2014) that develop in the walls of the production tanks of crustaceans and fish reduce the cost of production by minimizing the overload of waste components, consequently reducing water exchange (Pandey et al., 2014).
Even though bacteria in BFT and biofilm in tanks formation can be considered to be beneficial in aquaculture, it is notable that in small-scale laboratory cultures, bacterial loads at high densities may result in the mortality of planktonic organisms (e.g., phytoplankton and zooplankton) (Shishlyannikov et al., 2011). In the absence of dense organic matter, such as those in laboratory cultures, pathogenic microorganisms can adhere to cultured organisms (Torkildsen & Magnesen, 2004), and the intense aeration necessary to establish the BFT (Avnimelech, 2007) is unfeasible for cultures of smaller organisms, since the turbulence caused by the strong aeration could stress the organisms. Even if the laboratory culture has a high concentration of solids to which the microorganisms can adhere, this will cause a drastic consumption and reduction of dissolved oxygen because the volume of the medium is significantly lower than that of commercial cultures (Emerenciano et al., 2012). Also, the biofilm can eventually colonize the body and appendages of the cultivated organisms, resulting in a multitude of consequences for the basibiont, like: increased weight and friction, impeded trans-epidermal exchanges, altered color, smell and contour, resulting in multiple consequences. These changes may lead to the loss of buoyancy and motility, impair mating or even cause a substantial shift in the interactions among species (Wahl et al., 2012).
Both commercial and laboratory cultures can stimulate the selection and growth of opportunistic bacteria (Olafsen, 1993), resulting in diseases (Alday et al., 2006), lower production (Lipton et al., 2003), and consequently even the death of algae, invertebrates or fish (Wyban & Sweeney, 1991). The increased occurrence of diseases in aquatic species of economic interest due to the rapid multiplication of pathogens has resulted in significant losses in aquaculture, affecting the development of this sector in many countries (Pillay & Kutty, 2005). These diseases were principally caused by pathogenic microorganisms belonging to the bacterioplankton, mycoplankton, phytoplankton and protozoans (Uriarte et al., 2001). Among these microorganisms, the bacterioplankton is the one that can cause the most harm to aquatic species. Vibriosis and photobacteriose are the two most common types of bacterial diseases that can afflict marine, estuarine and sometimes freshwater farming systems and are principally responsible for the greatest impacts already reported in aquaculture (Defoirdt et al., 2007). In addition to the damage posed by the presence of bacterioplankton and mycoplankton in cultures, these microorganisms also interfere in aquatic scientific experiments, generating methodological problems that will be reflected on results (Spencer, 1952; Yetka & Wiebe, 1974), or making it impossible to test hypothesis about the role of bacteria and fungi in an ecosystem or community (DeLorenzo et al., 2001; Trottet et al., 2011).
Solutions for microbial control in cultures
Despite many years of research, bacterial and fungal loads are still a primary concern in the production and culture of planktonic organisms (Torkildsen & Magnesen, 2004) with several methods and techniques developed in an attempt to inhibit bacterial and fungal growth in cultures. According to Couch (1939) and Vieira (1977), the control of temperature, inoculum size, pH, the organic content of the medium, washing the cells (using filtration and centrifugation) and reisolation, are the main techniques used to inhibit and/or eliminate bacteria and fungi from cultures. Furthermore, these microorganisms can be controlled through sterilization by ultraviolet light (UV) (Rentachler et al., 1941; Alexandre et al., 2008), membrane filtration (Bobbitt & Betts, 1992; Zhou et al., 2011), autoclaving the water (Ferris & Hirsch, 1991; Creswell, 2010), detergent (McCracken, 1989) or through chlorination (Creswell, 2010; Liu et al., 2012). These methods can be used singly or in combination.
However, when the research involves the production and/or culture of live organisms, it is difficult to avoid contamination of sterile water through the air because microalgae or zooplankton cultures/production involve transferring and/or handling organisms at distinct time intervals (Lourenco, 2006; Agostini, 2014; Agostini et al., 2016).
Currently, the use of probiotics to inhibit the growth of pathogenic bacteria has been proposed as an important nutritional factor influencing gastrointestinal physiology and function in aquaculture (Diplock et al., 1999), and it was defined as a live microbial feed supplement that could beneficially affect the host animal by improving its intestinal balance (Fuller, 1989). However, these measures have rarely, if ever, completely prevented the incidence of infectious diseases in farm animals. According to Alday et al. (2006), with the possible exception of ranching, some degree of the antimicrobial cover has been necessary for all animal production systems with probiotics. Antimicrobial agents can be defined as natural, semisynthetic or as synthetic substances that can kill (bactericides and fungicides) or inhibit the growth of microorganisms (bacteriostatic, fungistatic), principally based on the action mechanism and concentration dose (Dixon, 2000). After the discovery of penicillin by Fleming in 1928, antibiotics have become important drugs for human and animal welfare.
Antibiotics should be safe (non-toxic) for the host, allowing their use as chemotherapeutic agents for the treatment of infectious bacterial diseases. In addition to their use in human and veterinary, antimicrobials are also used in cultured animals for human consumption, and their use can be categorized as therapeutic, prophylactic or metaphylactic (Serrano, 2005). According to Shaw et al. (1994) and Campa-Cordova et al. (2006), there are advantages to the application of antimicrobials to the control of microbial density in culture mediums relative to other methods, and the main ones include the ease of handling and implementation, as well as the maintenance of its effect on the artificial environment. Shishlyannikov et al. (2011) and Agostini et al. (2016) believe that the sole use of antimicrobials is possible to obtain bacteria and fungi-free cultures without damage to non-target organisms.
The importance of healthy and well-established cultures of planktonic organisms are a goal on a variety of scientific (biology and ecology) or economic studies focused on genetic, cytology, morphology, physiology, taxonomy, ecology and as a food source for aquaculture or human use. For this reason, we reviewed antibiotic and antifungal methods that have been used to obtain zooplanktonic and phytoplanktonic cultures free of bacterioplankton and mycoplankton. These procedures are widely dispersed in the literature. We now summarize them to establish an accessible guide to new scientists about the use of antimicrobials in the culture medium of planktonic organisms for i) assisting ecology studies to answer questions about the role of bacteria and fungi in aquatic communities, ii) enhancing or treating cultures of planktonic organisms used as food in aquaculture, and iii) facilitating biological studies (genetic, taxonomy, development, growth) preventing bacterial and fungal growth, without causing damage to non-target organisms.
Antimicrobials in planktonic cultures: historic
The use of prokaryote inhibitors (such as antibiotics) to control bacterial growth in cultures of planktonic organisms began in the 1940s, when penicillin was used to obtain bacteria-free cultures of the protozoan Tritrichomonas foetus (Riedmuller, 1928) (Ithaca & Mahmoud, 1944), and their use increased after the discovery of streptomycin in 1943, tetracycline in 1945 and neomycin in 1949. Between 1950 until 1969 there was an increase in the number of studies on this topic (Fig. 1). A series of papers documented the negative correlation between bacterial density and survival, and development of mollusk larvae (Loosanoff & Davis, 1963), leading to studies regarding the use of antibiotics in planktonic cultures of other organisms such as microalgae and crustaceans (Shaw et al., 1994; Agostini et al., 2016).
From the 1970s until 1999, the use of antimicrobials in cultures of planktonic organism cultures declined with the application of other chemicals to culture ponds due to the contamination of the environment, of the final product, or both (Collier & Pinn, 1998) (Fig. 1). From 2000 onwards, the problems concerning the use of antibiotics in aquaculture continued. However, a new field of application arose with studies using antibiotics and/or antifungals to acquire controlled environments free of microorganisms, enabling the test of hypotheses involving the contribution of bacterioplankton and mycoplankton in aquatic communities (DeLorenzo et al., 2001; Fouilland et al., 2007; Trottet et al., 2011) (Fig. 1).
A review on this topic using specialized books (Ray, 1966; Walne, 1970; Roberts, 1972; Brown, 1973; Kinne, 1977; Ukeles, 1977; Hetrick et al., 1981; Olafsen, 1993; Dixon, 2000; FAO/WHO, 2002; Pillay et al., 2005; Serrano, 2005; Alday et al., 2006; Lourenco, 2006; Creswell, 2010) and trough ASFA database (http://www.fao.org/fishery/asfa/en) using the keywords: plankton and antibiotics and antifungal, plankton and antimicrobials, aquaculture and bacteria-free returned 204 publications between 1940 and 2016 related to the use of antimicrobials in planktonic cultures. Google scholar (https://scholar.google.com.br) and CAPES periodic portal (http://www.periodicos.capes. gov.br) were also used to complement the information. From the review, it was seen that the decades starting on the 1960s and 2000 were the ones when most of the papers on this topic were published, corresponding each with 25.5% of the retrieved papers. The lowest number of publications goes back to the 1940s (2.2%), at the beginning of this line of study, and when the associated problems in aquaculture arose in the 1990s (7%). Fifty-seven antimicrobial agents were applied to plankton cultures between 1940 and 2016 (Annex 1).
The reviewed material indicated that the application of antibiotics in cultures not only ensures the inhibition of bacterial growth but also accelerates the development of the species of interest and increases their survival, when compared to control without antibiotics, reinforcing the idea that these substances may also be used as a tool for the hypothesis test. It was also observed that penicillin and streptomycin were the most often used in cultures of planktonic organisms; however, the percentage used about published works has decreased (Fig. 2), probably due to the discovery/formulation of new antibiotics. Currently, there is increased use of chloramphenicol (Chloromycetin[R]), oxytetracycline and neomycin in studies. These antimicrobials, together with penicillin and streptomycin, are the five antibiotics that are most often used (Fig. 2) due to their greater efficiency in inhibiting the bacterial community (bacterioplankton) (Annex 2) and when used in combination, ensure a broad spectrum of bacterial inhibition. Thus, antimicrobials could be associated with peptides (tryptone), acids (oxolinic, nalidixic), surfactants (Tween-80) or detergents (Eggermont et al., 2014). Guillard (2005) recommends the addition of organic matter with low molecular weight (for example, 0.006 mg [L.sup.-1] glucose) when using antibiotics because this will ensure the inhibition of the synthesis of the bacterial cell wall. If bacterial growth is not happening, antibiotic will only retain the inert cells; on the other hand, if the biosynthesis of cell walls were occurring, will result in fatal bacterial damage.
Some authors emphasize that when successfully inhibiting bacteria, the niche is usually occupied by filamentous fungi and/or yeasts, which, in most cases, also needs to be controlled by applying an antifungal to avoid ill effects to the organisms of interest (Agostini, 2014; Agostini et al., 2016). Considering that most fungal pathogens are secondary or opportunistic invaders, which already belong to the biota of the water used, they can cause problems to farmed organisms (Leano et al., 2005), e.g., mycoses, that have been considered one of the main factors related to economic losses in aquaculture (Zaror et al., 2004). Therefore, fungi can cause as much damage as bacteria; however fungi contamination is less common in marine than freshwater cultures (Lourenco, 2006).
The main antifungal agents used in cultures of planktonic organisms in the period between 1940 and 2016 included nystatin (51%), cycloheximide (30%), amphotericin-B (14%) and candicidin (5%) (Fig. 3). Many authors reported nystatin (Micostatin[R]) for the inhibition of fungal growth of filamentous fungi and yeasts in cultures (Lee et al., 1970; Sande & Mandell, 1987; Groll et al., 1999; Wilkens & Maas, 2012). This antifungal was first discovered in the early 1950s and is produced by the growth of the bacteria Streptomyces noursei. This antifungal bind to ergosterol in the plasmatic membrane of the fungal cell, forming pores that will lead to the loss of K as well as other small molecules to the medium, causing the death of the fungus (Lourenco, 2006). Cycloheximide is another often used antifungal, that will inhibit the protein synthesis in eukaryotes, by preventing the elongation of peptides through the transferal peptidase activity in ribosomes 60S (Lourenco, 2006). It is also produced by a bacteria, namely Streptomyces griseus, and was first used by Ray (1966) in cultures of the oyster Crassostrea virginica. Another antifungal, amphotericin-B (Fungizone[R]), was originally extracted from Streptomyces nodosus in 1955, and employed by Lee et al. (1970) in combination with antibiotics in nematode cultures to inhibit filamentous fungi. Candicidin is an antifungal compound obtained from Streptomyces griseus and was only used by Provasoli & Gold (1962) in cultures of the protozoan Crypthecodinium (=Gyrodinium) cohnii (Seligo) Javornicky, 1962 in combination with antibiotics. Both amphotericin B and candicidin have the same active principle of nystatin (Lourenco, 2006).
Combining antibiotics and antifungals could be an alternative to maintain or reduce the initial bacterial load and thus reducing the risk of handling contamination; however, using these substances to prevent bacterial and fungal infections should be done carefully to avoid harming the organisms of interest (Trottet et al., 2011).
Antimicrobials in planktonic cultures: major contributions
Antimicrobial and other chemical agents have been used in conjunction with physical methods for many years to obtain axenic cultures of planktonic organisms. These procedures are widely dispersed in the literature since the 1940s. The present report summarizes this information for researchers that needs to minimize bacterial proliferation in planktonic cultures. The majority of the papers published between 1940 and 2016 regarding the areas of application for antimicrobial agents (Annex 3) were related to the inhibition of bacteria and fungi in cultures/production of phytoplankton (e.g., Campa-Cordova et al., 2006), followed by crustaceans (e.g., Agostini et al., 2016), hypothesis testing involving the planktonic community (e.g., Trottet et al., 2011), mollusks (e.g., Roberts et al., 2007), protozoan (e.g., Provasoli & Gold, 1962), fish (e.g., Struhsaker et al., 1973), planktonic phase of seaweed (e.g., Kobayashi et al., 2003), periphyton (spores can be found in planktonic enviromental) (e.g., Vieira, 1977), Rotifera (e.g., Dougherty et al., 1960), Cnidaria (e.g., Claybrook & Eakin, 1960), Cyanobacteria (e.g., Guo & Chen, 2012), tychoplanktonic nematodes (zooplankton that oscillate periodicaly their position in water column) (e.g., Lee et al., 1970), Porifera (e.g., Borojevic, 1966), Platyhelminthes (e.g., Miller & Johnson, 1959) and meroplanktonic Nemertea (zooplankton with a life cycle splited in pelagic and benthic enviromental) (e.g., Tuker, 1959) (Fig. 4).
We believe that the major use of antimicrobials in cultures of planktonic microorganisms i) allow/improve the culture of planktonic organisms and ii) increase our knowledge about the role of bacteria and fungi in aquatic communities, testing hypothesis. Through the use of specific inhibitors in planktonic cultures, it is possible to i) eliminate or decrease bacteria and/or fungi load in the medium (Youn & Hur, 2007), ii) inhibit the growth of pathogenic microorganisms (Castro-Mejia et al., 2007), iii) increase zooplankton and phytoplankton growth/survival (Campa-Cordova et al., 2006), development (Uriarte et al., 2001) and production (Agostini, 2014), and iv) reduce competition between phytoplankton and bacterioplankton (Youn & Hur, 2007) and eliminate bacterial aggregates on microalgae wall's (Vieira, 1977). In phytoplankton and periphyton cultures, Vieira (1977) compare different methods and antimicrobials to maintain cultures of 12 different species of microalgae bacteria-free. He noted that the use of antibiotics boosted results. However, some criteria such as i) the evaluation of the physiological state of the algae cells to be treated (algal cells in the decline phase of growth are strongly attacked by bacteria, and are more sensitive to chemicals substances), and ii) the sensitivity of microalgae to antimicrobials (which varies according to the species, antibiotic, concentration and exposure time), should be followed to ensure the success of the method. Similarly, Youn & Hur (2007) determined the extent of bacteria contamination and resistance to various antibiotics commonly used in different microalgal cultures (Chlorella ellipsoidea Gerneck, 1907; Isochrysis galbana Parke, 1949; Heterosigma akashiwo (Hada) Hada ex Hara & Chihara, 1987; and Cyclotella didymus and Thalassiosira alleni Takano, 1965). Seven different dosage levels of chloramphenicol, dihydrostreptomycin sulfate, neomycin, penicillin G, streptomycin sulfate, penicillin G + streptomycin sulfate and penicillin G + streptomycin sulfate + chloramphenicol were added to each culture of microalgae. The authors verified that axenic culture of Bacillariophyceae and Dinophyceae was more difficult to obtain than those of Chlorophyceae and Haptophyceae because of them intricated external morphology. The efficiency of different antibiotics and their concentrations to obtain axenic cultures varied depending on the microalgal species used. The same conclusion was also observed by Vieira (1977).
For zooplankton cultures, the findings of Walne (1956, 1958, 1963, 1970) on molluscan production encouraged the application of antimicrobials in other zooplankton cultures (i.e., heterotrophic protozoans, rotifers, crustaceans and fish). This author used antibiotics (penicillin + streptomycin) to benefit oyster, through direct application in the culture medium and food (microalgae) of this molluscan in order to eliminate pathogenic microorganisms and increase the survival of oysters (More information in zooplankton cultures can be seen in Annex 2.2).
Regarding hypotheses tests, Muller (1969) initiated the use of antibiotics for test ecological relationship on the biofouling process, however involving just one planktonic invertebrate species (Hydractinia echinata (Fleming, 1828)). While Yetka & Wiebe (1974) used specific inhibitors in an aquatic laboratory system, involving all community, without success because they concluded that the antibiotics tested could not be used to delineate bacterial respiration in mixed microbial communities. However, this initial approach leaded Sherr and collaborators in 1986 to estimate the grazing rates of heterotrophic nanoplankton on bacterioplankton using inhibitors, as well as Wheeler & Kirchman (1986) to evaluate the utilization of inorganic and organic nitrogen by bacteria in marine systems applying antimicrobials in the medium, thus opening the way for other research using antimicrobials in different fields. For example, Maurin et al. (1997) evaluated the relationship between phytoplanktonic excretion and bacterial reassimilation in an oligo-mesotrophic lake, using antibiotics to get treatment without bacteria, making it possible to prove the hypothesis that bacterial heterotrophic reassimilated most of the products excreted by phytoplankton. Meanwhile, Bidle et al. (2003) experimented in paleoceanography area with treatment with antibiotics to prove that marine bacteria accelerate biogenic silica dissolution rates in the sea.
In aquatic ecology, the main contributions on the application of antimicrobials for hypothesis tests were the works of DeLorenzo et al. (2001) and Trottet et al. (2011). DeLorenzo et al. (2001) use of metabolic inhibitors (penicillin+streptomycin+neomycin+cycloheximide) to characterize ecological interactions of the com-munity (free-living and adherent heterotrophic bacteria, ciliate and flagellate) in an estuarine microbial food web proved their hypotheses that there are seasonal shifts in microbial food web structure and function related to the season. In their study, they showed the important role of microbial loops in driving primary and secondary production in estuaries, using antimicrobials as a tool. Trottet et al. (2011) selected, tested and compared the most commonly reported antibiotics to assess their effect on bacterial growth and functional diversity of natural communities and their efficiency involving phytoplankton and bacterioplankton interactions such as competition and mutualism, or lack of interaction between the different components of the microbial communities to study their relative importance in biogeochemical fluxes. They found that penicillin and streptomycin at a final concentration of 0.1 g [L.sup.-1] each significantly reduced bacterial growth within two hours. They also reported that there was a greater impact on bacterial functional diversity when both antibiotics were mixed, and this mixture did not have any significant effect on the growth of selected cultured phytoplankton strains. The most interesting aspects of these works is the community level study (DeLorenzo et al., 2001) which differs from those that evaluated the interaction of bacterioplankton with only one functional group (i.e., phytoplankton) and the comparison of different antimicrobials (individually or in combination) (Trottet et al., 2011).
While in population level, Shaw et al. (1994) used antibiotics with success as tools to evaluate situations in which marine phytoplankton use chemical feeding deterrents to reduce or inhibit grazing by the copepod Tigriopus californicus (Baker, 1912). Whereas Tartarotti & Torres (2009) used treatments with the antibiotic gentamicin (50 g [L.sup.-1]; applied at a concentration of 1 mL [L.sup.-1]) in cultures of the copepod Acartia tonsa Dana, 1849 to successfully test the hypothesis that bacteria affect the formation of the copepod exoskeleton. Although it is noteworthy that prokaryotic and eukaryotic inhibitors have been successfully used also to evaluate: i) the role of bacteria in the production of metabolites (Ringelberg & Van Gool, 1998), ii) the role of microbes in the decomposition process (Tang et al., 2006), iii) phytoplankton-bacteria interactions (Hamdan & Jonas, 2007), iv) competition for dissolved nitrogen (Fouilland et al., 2007), v) influence of bacterioplankton activities on nitrogen uptake rates (Tungaraza et al., 2003), vi) interaction on biofouling process (Roberts et al., 2007) and vii) the potential protein synthesis by bacteria (Tartarotti & Torres, 2009).
Adverse effects of antibiotic use on cultures
Despite all these benefits, due to improper disposal, the development of bacterial resistance and ecological problems, the current trend is to reduce the use of antibiotics. Furthermore, import restrictions by the presence of residues in tissues of cultured organisms and possible damage to public health, result even in the banning and limitation of the use of these antimicrobials in many countries when used in cultures of organisms for human consumption (Defoirdt et al., 2007). Antimicrobial agents are usually administered to marine fish (Buschmann et al., 2012), and its feces containing unabsorbed antimicrobials and secreted antimicrobial metabolites in the environment of fish farming sites often retain their antimicrobial activity and can remain in the aquatic environment for variable periods (Burridge et al., 2010). For example, McCracken et al. (1976) established that the antibiotic trimethoprim could remain in the system for 77 days after the cessation of treatment. Therefore, environmental contamination can occur if the tank water is discharged into the environment within this period.
Antibiotics act as inducers of bacterial genes encoding mechanisms of drug resistance (Butaye et al., 2003) and the selection of antimicrobial-resistant bacteria in the marine environment could have detrimental impacts on animal and human health (Buschmann et al., 2012). Nevertheless, there is a hypothesis that antibiotics resistance varies between environments and regions, depending primarily on the selection pressure imposed on the ecosystem (Pereira et al., 2006), and the selection power is proportional to the exposure time of the bacteria to the antimicrobial (Aliabadi & Lees, 2000).
Antibacterial agents have been frequently detected in sewage effluents, surface waters and groundwater (Ying & Kookana, 2007) through the improper disposal of water with antimicrobial residues (by aquaculture, hospital, industrial and domestic sewage). According to Hektoen et al. (1995), a large portion of the antibiotics administered in farms (70-80%) has been reported to reach the environment, promoting the impact of the disposal on the adjacent community. Moster (1986) observed detectable levels of antibiotic in blue mussels (Mytilus edulis) located 80 m from a fish farm where antibiotics were used. The ecological effects in the environment are related to the lack of biodegradation of these substances. Only a few of the compounds were partially biodegraded in aquatic systems (Kummerer et al., 2000), accumulating in the water and sediment and this allows the appearance of resistant bacteria to affect the food chain directly (Kummerer, 2003). For example, according to Lourenco (2006), continuous exposure to antibiotics generates damage with various extensions in microalgae. Thus, this author suggests only short-term treatments. Furthermore, it is reported in the literature that the use of antibiotics can cause in planktonic organisms: genetic mutations (Kumar, 1964; Droop, 1967), inhibiting the nuclear DNA synthesis in algae (Vieira, 1977), loss of color in microalgae and protozoa (Provasoli et al., 1948), inhibition of chloroplasts (Vieira, 1977) and mitochondrial synthesis (Lloyd, 1974) in algae, abnormalities in the morphology and behaviour of the clam larvae (Fitt et al., 1992), toxicity (Wollenberger et al., 2000) and inhibition of growth (Kviderova & Henley, 2005).
As noted in section 1.2.1, the use of probiotics (live microorganisms that when administered in adequate amounts confer a health benefit for the organism cultivated, inhibiting possible pathogens) (FAO/WHO, 2002) can be a solution for large-scale cultures destined for human consumption, replacing the use of antimicrobials. Rego et al. (2012) observed that the concentration of Vibrio spp. on the water and postlarvae, shrimps of Litopenaeus vannamei were significantly reduced with the use of Bacillus spp. probiotic. Riquelme & Avendano-Herrera (2003), for example, used streptomycin/oxytetracycline + furaltadone to compare the efficiency of probiotics for the same species culture. Probiotics had the same results regarding mollusk survival than antibiotics; however, the antibiotic treatment decreased bacterial density more than probiotic treatment, being the most indicated for the hypothesis test, that requires a culture medium with minimum bacteria as possible. Still, short-time cultures without transfer of organisms and with low organic matter can be maintained without bacterial and fungal contamination by traditional methods (sterilization, chlorination or filtration of the culture medium), preferably maintaining the cultures covered (i.e., PVC film), but with light penetration, avoiding contamination via air, in order to maximize antimicrobial efficiency.
There are other chemical procedures for the purification of marine and freshwater cultures, particularly of microalgae, involving the use of bacteriostatic agents such as potassium tellurite ([K.sub.2]Te[O.sub.3]) or sulfonamides, which oxidizes bacterial cells and prevents the synthesis of nucleic acids by bacteria, respectively. Besides the application of the enzyme lysozyme, iodine in alcoholic solution or ionic detergent (Triton and Tween), as well as of Dakin's solution (0.45 to 0.5% sodium hypochlorite + 4% boric acid) developed during the First World War (Lourenco, 2006). The problem with these methods is that they often need to be applied in conjunction with antimicrobial or accompanied by physical procedures (i.e., washing and centrifuging) to ensure its efficiency.
Future directions: remarks and conclusion
Planktonic organisms are involved in the major ecosystem processes in the aquatic community. However, ecological laboratory studies require precise and replicable protocols that allow the understanding of the biological and ecological factors that directly and indirectly affect a population or a community, respectively, without affecting organisms of interest. The application of antimicrobials in laboratory cultures of planktonic organisms seems to be an alternative to obtain responses at the population level or the community level without the microbial influence, although care must be taken to obtain accurate results. A pilot investigation on the characteristics and effects of antimicrobials should be conducted to obtain precise results, ensuring maximum efficiency of antimicrobials in the aquatic system. According to McCracken (1989), there is no overall applicable method for all species because every culture has different communities of microorganisms and the degree of sensitivity of organisms may show different responses to the same chemical. Thus, we have established remarks for the use of antimicrobials in planktonic cultures safely either for the hypothesis test or to obtain healthy cultures:
i) Penicillin, streptomycin, oxytetracycline and neomycin are the antibiotics most often used in planktonic cultures with success, individually or in combination and they must be prioritized in the choice, either for phytoplanktonic or zooplanktonic organisms.
ii) Note the tolerance of the organisms to the antimicrobial chosen. Give preference to antibiotic combinations of a broad spectrum, because studies indicate that they are more efficient than individual antimicrobials alone (Pappas & Hoffmann, 1952; Kinne, 1977; Agostini et al., 2016). However, attention should be paid to the burnout effect among them. Speck et al. (1951) reported that chlortetracycline (Aureomycin[R]) and oxytetracycline (Terramycin[R]) antagonized the action of penicillin in cultures. Furthermore, the antagonistic effects between species that can minimize the effects of antibiotics used must also be checked. Tchan & Gould (1961) found that bacteria tested alone were sensitive to some of these antibiotics, but not when associated with the blue-green algae, suggesting a protective effect of the algae.
iii) In the development of bacteria-free cultures, previous sterilization of the equipment, such as glassware and medium, will probably be beneficial, because this will reduce the initial bacterial load (Alexandre et al., 2008; Creswell, 2010; Zhou et al., 2011). Cover the cultures (e.g., PVC film) could also be an alternative to avoid contamination.
iv) The stock solution of antimicrobials (diluted in distilled water) must be prepared, if possible, immediately before use; otherwise, it must be frozen after being filtrated trough sterilized filters (0.2 [micro]m). Two variables define the final result: the dose of the antimicrobial and the exposure time (Lourenco, 2006).
v) Evaluate the effectiveness of the selected antibiotics through bacterial density estimated by checking the onset of action and its half-life in the culture medium.
vi) Test the antimicrobials previously in the salinity and culture medium of interest, since studies have shown that the variation of the salinity medium results in an increase of the toxicity of the chemical substances in invertebrates (Kwok & Leung, 2005; Pedroso et al., 2007), due to alteration of the water content and concentration of inorganic ions (Ferguson & Hogstrand, 1998).
vii) The use of the appropriate antibiotics will result in the inhibition of bacteria in the culture medium. However, this will likely cause an overgrowth of fungi, making it necessary to include a small concentration of a eukaryotic inhibitor in the combination after a previous sensitivity test. Tang et al. (2006), Agostini (2014), and Agostini et al. (2016) reported the prevalence of fungi when the bacterial load was reduced, suggesting the inclusion of an antifungal. We suggest the application of nystatin (the antifungal most often used in cultures), but in low concentration, because this inhibits eukaryotes organisms.
viii) There may be different sensitivities to the same treatment of antimicrobial between development stages of the same animal species; usually, earlier stages are more sensitive. For the adult mollusk Ostrea edulis Linnaeus, 1758, for example, 0.25 g [L.sup.-1] of streptomycin in combination to 50,000 IU [L.sup.-1] of penicillin is applied in its culture medium (Walne, 1963), however for larval stages just 0.05 g [L.sup.-1] of streptomycin + 50,000 IU [L.sup.-1] of penicillin will be required (Walne, 1958). For egg culture of the barnacle Fistulobalanus albicostatus, Chen et al. (2007) suggest the use of 0.01 g [L.sup.-1] of penicillin + 0.005 g [L.sup.-1] of streptomycin, however for barnacle larvae of the same species it is advisable to use 0.02 g [L.sup.-1] of penicillin + 0.03 g [L.sup.-1] of streptomycin (Yoshimura et al., 2006). For this reason, even if the combination of antimicrobials has been utilized for the cultivation of an adult of a particular species, it is advisable to test this treatment with the development stage of interest.
ix) It is necessary to evaluate the water quality (ammonia, nitrite, nitrate, phosphate, sulfate) and estimate possible changes in the use of antimicrobials in culture medium caused by the withdrawal of bacteria. The bacterioplankton is responsible for nutrient cycling, and its removal could result in the accumulation of nutrients to toxic levels (Alongi, 1994; Silva et al., 2012).
x) Make sure to process and appropriately dispose of the culture and the production medium with antimicrobials avoiding environmental contamination and/or bacteria resistance.
Even with the limitations in the application of antimicrobials in farming systems intended for human consumption, these substances have the potential to be used in controlled laboratory cultures of planktonic organisms intended to be used in bioassays, and also for testing hypotheses aimed at evaluating the contribution of the bacterial and/or fungal in the aquatic community (DeLorenzo et al., 2001; Trottet et al., 2011; Agostini et al., 2016). Therefore, with proper care, scientists may use these substances in scientific experiments where systems without bacterioplankton and/or mycoplankton contamination are needed to provide a better understanding of the real effect of the microbial community such as competition and mutualism, or the lack of interaction between the different components of the planktonic community. Besides, it could be used to assess the relative importance of these microorganisms in biofouling, marine snow, biogeochemical fluxes, microbial loop, benthic-planktonic coupling and the biological pump.
ACKNOWLEDGMENTS
The authors acknowledge the support of Federal University of Rio Grande and Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq-141217/2014-6) and PRONEM FAPERGS/CNPq 11/2014 (6/2551-000244-4).
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Vanessa Ochi Agostini (1,3,4), Lais Fernanda De Palma Lopes (1,3,5) Alexandre Jose Macedo (2) & Erik Muxagata (1)
(1) Laboratorio de Zooplancton, Instituto de Oceanografia, Universidade Federal do Rio Grande Rio Grande, RS, Brasil
(2) Laboratorio de Biofilmes e Diversidade Microbiana, Faculdade de Farmacia and Centro de Biotecnologia Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brasil
(3) Programa de Pos-graduacao em Oceanografia Biologica, Schollarship from Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq)
(4) Laboratorio de Microcontaminantes Organicos e Ecotoxicologia Aquatica Postdoctoral fellow from Coordenacao de Aperfeicoamento de Pessoal de Nivel Superior at Programa de Pos-Graduacao em Oceanologia, IO, FURG
(5) Programa de Pos-graduacao em Ciencias da Engenharia Ambiental, Schollarship from CAPES Nucleo de Ecotoxicologia e Ecologia Aplicada, Universidade de Sao Paulo, Sao Carlos, SP, Brasil Corresponding author: Vanessa Ochi Agostini (voagostini@gmail.com)
Corresponding editor: Eduardo Ballester
Received: 15 September 2017; Accepted: 4 April 2019
DOI: 10.3856/vol47-issue3-fulltext-2
SUPPLEMENTARY DATA
Annex 1. Main antimicrobials (prokaryote inhibitors) used in plankton
cultures between 1940 and 2016.
Used between 1940
Antimicrobials and 2016 (%) 1940-1959
Aerosporin 0.2
Amoxicillin 0.9
Ampicillin (Binotal[R]) 1.6
Basitracin 0.7 X
Carbenicillin (Geopen[R]) 0.5
Cefazolin 0.2
Cefuroxime 0.3
Cephalothin (Keflin[R]) 0.5
Chloramphenicol (Chloromycetin[R]) 9.5 X
Chlortetracycline (Aureomycin[R]) 3.2 X
Ciprofloxacin 1.4
Colomicin 0.5
Dihydroestreptomicine 2.9 X
Doxycycline 0.2
Enrofloxacin 0.5
Erythromycin
(Clarithromycin[R], Iloticina[R]) 3.2 X
Florfenicol (Nuflor[R]) 0.3
Furaltadone 0.5
Furazilidone 0.2
Gentamicin 1.4
Gramicidin 0.7 X
Imipenem 0.7
Kanamycin 1.4
Levofloxacin 0.2
Lincomycin 0.5
Neomycin 4.3 X
Nitrofurantoin 0.2
Norfloxacin 0.9
Novobiocin 0.7 X
Ofloxacin 0.2
Oxytetracycline 4.1 X
Penicillin 23.9 X
Polymyxin-B 1.6 X
Pyrimethamine 0.2
Rifampicin 0.5
Ristocetin 0.2
Roxithromycin 0.3
Spiramycin 0.2
Streptomycin 18.5 X
Sulfamerazine 0.5
Sulfamethoxazole 1.1
Sulfonamide, (Sulfadiazine[R],
Sulfadimethoxine[R]) 1.1
Tetracycline 3.2 X
Thiamphenicol 0.5
Triclocarban 0.3
Trimethoprim 2.0
Trisulfapyrimidine
(Triple sulfa[R]) 0.2
Tylosin 0.9
Vancomycin 0.9 X
Years
Antimicrobials 1960-1989 1990-2016
Aerosporin X
Amoxicillin X
Ampicillin (Binotal[R]) X X
Basitracin
Carbenicillin (Geopen[R]) X
Cefazolin X
Cefuroxime X
Cephalothin (Keflin[R]) X
Chloramphenicol (Chloromycetin[R]) X X
Chlortetracycline (Aureomycin[R]) X X
Ciprofloxacin X
Colomicin X
Dihydroestreptomicine X X
Doxycycline X
Enrofloxacin X
Erythromycin
(Clarithromycin[R], Iloticina[R]) X X
Florfenicol (Nuflor[R]) X
Furaltadone X
Furazilidone X
Gentamicin X X
Gramicidin
Imipenem X
Kanamycin X
Levofloxacin X
Lincomycin X
Neomycin X X
Nitrofurantoin X
Norfloxacin X
Novobiocin X
Ofloxacin X
Oxytetracycline X
Penicillin X X
Polymyxin-B X
Pyrimethamine X
Rifampicin X
Ristocetin X
Roxithromycin X
Spiramycin X
Streptomycin X X
Sulfamerazine X
Sulfamethoxazole X
Sulfonamide, (Sulfadiazine[R],
Sulfadimethoxine[R]) X X
Tetracycline X X
Thiamphenicol X
Triclocarban X
Trimethoprim X
Trisulfapyrimidine
(Triple sulfa[R]) X
Tylosin X
Vancomycin X X
Annex 2. Inhibiting concentrations (g [L.sup.-1]) of the five most
frequently cited antibiotics for different bacterial strains (modified
from Berland & Maestrini, 1969; Lourenco, 2006). *Partial activity.
Antibiotic
Bacterioplakton species Penicillin Streptomycin Chloramphenicol
Action Gram + Gram [+ or -] Gram [+ or -]
Pseudomonas aestumarina 4 >10 1
Psedomonas cruciviae 0.001 0.03 0.002
Pseudomonas marinoglutinosa 2.5 4 0.15
Pseudomonas riboflavina 0.05 0.02 0.025
Pseudomonas stereotropi s 0.00025 0.025 0.002
Vibrio algosus 1.75 0.003 0.01
Vibrio phytoplanktis 0.015 0.08 0.0015
Agarbacterium mesentericus 3 0.02 0.005
Xanthomonas 0.03 >10 0.001
Achromobacter parvulus 0.001 >10 0.002
Achromobacter stationi s 0.00025 0.015 0.0015
Achromobacter stenohalis 0.05 0.005 0.0015
Flavobacterium aquatile 0.05 0.04 0.03
Flavobacterium l ut escens 1 >10 0.075
Flavobacterium peregrinum 0.002 10 0.005
Micrococcus 0.015 0.025 0.002
Staphylococcus aureus 0.007 0.02 0.005
Antibiotic Mechanism of action
interferes with the synthesisofbacterial
cellwall by inhibiting enzymesinvolved in
Penicillin G transpeptidation, making them fragile and
subject to rupture
Streptomycin interrupts bacterial growth by binding to
the 16S rARN subunit, preventing the
synthesis
of polypeptide chains
inhibitsthe activityof the enzyme peptidyl
transferase, preventing the coupling of
Chloramphenicol amino-acyl-rARN to the site of the 50S
subunit of the ribosome, preventing
bacterial
protein synthesis
inhibits cell growth by preventing
translation: coupled to the part of the
16S subunit of
Oxytetracycline 30S ribosomes and prevents the action of
amino-acyl-tARN in the site A of organelle
prevents the translocation site acyl
peptidyl-tARN to the site A to site P
resulting in
Neomycin mRNA reading errors which lead to the
interruption of protein synthesis
Bacterioplakton species Oxytetracycline Neomycin
Action Gram [+ or -] Gram [+ or -]*
Pseudomonas aestumarina 2 0.02
Psedomonas cruciviae 0.05 0.03
Pseudomonas marinoglutinosa 1 1
Pseudomonas riboflavina 0.02 0.02
Pseudomonas stereotropi s 1.75 0.05
Vibrio algosus 1.5 2
Vibrio phytoplanktis 1.7 1.75
Agarbacterium mesentericus 1.5 0.03
Xanthomonas 1 1.5
Achromobacter parvulus 1,5 1.25
Achromobacter stationi s 0.05 0.01
Achromobacter stenohalis 0.02 0.015
Flavobacterium aquatile 1.25 >10
Flavobacterium l ut escens 0.075 >2.1
Flavobacterium peregrinum 10 0.01
Micrococcus 2.5 4
Staphylococcus aureus 1.5 0.03
Antibiotic
Penicillin G
Streptomycin
Chloramphenicol
Oxytetracycline
Neomycin
Annex 3. List of important published papers on the use of
antimicrobials in culture/production and in hypothesis testing to
obtain a bacteria-free medium. *Unspecified.
Antimicrobials used Application
penicillin Trichomonas foetus
(protozoan)
* Trichomonas foetus
(protozoan)
penicillin Trichomonas foetus
(protozoan)
penicillin Protozoan
* Phytoplankton community
* Nematode
penicillin, dihydrostreptomycin Euglena gracilis
(protozoan)
aureomycin + oxytetracycline hydrochloride *
+ penicillin
streptomycin Ca[Cl.sub.2] + penicillin Nitzschia closterium
(periphyton)
penicillin Phytoplankton community
penicillin + streptomycin Euglena gracilis
(protozoan)
nystatin Phytoplankton community
penicillin + streptomycin Sardinops caerulea,
Gadus callarias,
Pleuronichthys sp.
(fish)
penicillin + streptomycin Oyster (mollusk)
penicillin Amphibalanus eburneus
(barnacle)
aureomycin *
penicillin + streptomycin Oyster (mollusk)
streptomycin Copepod
terramycin, streptomycin, polymyxin-B, Scenedesmus obliquus,
Chlorella pyrenoidosa,
Chlorella
tetracycline, penicillin, bacitracin, vulgaris (phytoplankton)
chloromycetin and gramicidin
penicillin Podophrya collini
(protozoan)
streptomycin Ramphogordius
sanguineus, Amphiporus
formidabilis
(nemertine)
aureomycin, chloramphenicol, tetracycline, Dugesia dorotocephata
(platyhelminthes)
streptomycin, neomycin, erytromycin,
novobiocin, vancomycin, penicillin,
trypaflavin, filipin
penicillin + streptomycin Ectopleura crocea
(Cnidaria)
chlortetracycline + chloramphenicol + *
streptomycin
bicyclohexylamine Hydra oligactis, Hydra
viridissima (Cnidaria)
penicillin + streptomycin Lecane inermis (rotifer)
penicillin Ectocarpus siliculosus,
Hincksia secunda
(seaweed)
nystatin Phytoplankton community
* Cyanobacteria
* Neurospora crassa
(Fungi)
chlortetracycline + citric acid Phytoplankton community
penicillin + streptomycin/ chloramphenicol Mercenaria mercenaria
(mollusk)
penicillin + dihydrostreptomycin Detonula confervacea,
Cyclotella nana 3H
(phytoplankton)
penicillin + chloramphenicol + neomycin + Gyrodinium cohnii
(protozoan)
polymyxin-B + dihydrostreptomicin +
tetracycline + candicidin
streptomycin, penicilin Calanus hyperboreus
(copepod)
penicillin + streptomycin Fed to Ostrea edulis
(mollusk)
amphotericin-B + streptomycin Phytoplankton community
penicillin + streptomycin Stylonema alsidii
(seaweed)
penicillin + chloramphenicol + neomycin + Gyrodinium resplendens
(phytoplankton)
polymyxin B
dihydrostreptomycin + streptomycin Mercenaria mercenaria,
Crassostrea virginica
(mollusk)
polymyxin-B + neomycin Diatom (phytoplankton)
chlortetracycline + citric acid Phytoplankton community
penicillin + streptomycin *
penicillin + streptomycin Mya arenaria (mollusk)
penicillin + streptomycin + chloramphenicol Acetabularia sp.
(seaweed)
penicillin + streptomycin Mytilus edulis (mollusk)
penicillin + streptomycin + chloramphenicol Tetraselmis maculata
(phytoplankton)
+ Tween-80
cycloheximide Crassostrea virginica
(mollusk)
penicillin + streptomycin Euterpina acutifrons,
Temora turbinata,
Oncaea sp. (copepod)
streptomycin, penicillin Calanus hyperboreus
(copepod)
penicillin + streptomycin Mycale contarenii
(Porifera)
penicillin + dihydrostreptomycin Penaeus aztecus (shrimp)
cycloheximide, oxytetracycline, Crassostrea virginica
(mollusk)
chlortetracycline, tetracycline
penicillin + streptomycin + chloramphenicol Mercenaria mercenaria
(mollusk)
sulfamethazine Crassostrea virginica
(mollusk)
streptomycin, penicillin Calanus hyperboreus
(copepod)
tetracycline, streptomycin, penicillin Invertebrates
chloramphenicol + chlortetracycline + *
streptomycin
chloramphenicol + streptomycin / penicillin Diatoms (phytoplankton)
+ streptomycin + neomycin +
chloramphenicol
penicillin + neomycin + nystatin Acetabularia acetabulum
(mediterranea) (seaweed)
penicillin + streptomycin Rhincalanus nasutus
(copepod)
penicillin + dihydrostreptomycin + nystatin Protozoan
chloramphenicol *
gentamicin *
penicillin + streptomycin Tintinnopsis tubulosa
(protozoan)
penicillin + streptomycin Tintinnopsis tubulosa
(protozoan)
neomycin + streptomycin Pinctada maxima
(mollusk)
* Hypothesis test with
Hydractinia echinata
(Cnidaria)
penicillin + streptomycin Deontostoma californicu
m (nematode)
penicillin + streptomycin Ulva (Enteromorpha)
linza, Cladophora
rivularis (gracilis)
(seaweed)
chloramphenicol + novobiocin Foraminifera (protozoan)
spiramycin, ristocetin, sulfamerazine, triple Diatom (phytoplankton)
sulpha, vancomycin, penicillin, streptomycin
penicillin + streptomycin Crepidula fornicata
and Nassarius
reticulatus (mollusk)
penicillin + carbenicillin + kanamycin + Acetabularia
mediterranea
(phytoplankton)
vancomycin
novobiocin + erythromycin, novobiocin + Nematode
colimycin + nystatin, novobiocin + colimycin
+ fungizone
penicillin + streptomycin Elminius modestus
(barnacle)
penicillin Euterpina acutifrons
(copepod)
penicillin + streptomycin Oyster (mollusk)
chloramphenicol *
penicillin Callinectes sapidus
(crab)
penicillin + streptomycin + chloromycetin Invertebrates
dihydrostreptomycin, binotal *
several Review (invertebrates)
penicillin + gentamicin + streptomycin Phytoplankton
penicillin + chloramphenicol + neomycin + Oscillatoria sp.,
Pediastrum boryanum,
Chlorella vulgaris
penicillin + tetracycline + chloramphenicol + (phytoplankton)
aureomycin + ceporin + neomycin
colimycin, geopen + carbenicillin, penicillin, Fish
penicillin + ampicillin, keflin + cephalothin,
aerosporin
erythromycin, carbenicillin, penicillin, Caranx mate (fish)
ampicillin, cephalothin, nitrofurantoin,
sulfadiazine
chloramphenicol + colimycin Foraminifera (protozoan)
colimycin, streptomycin, penicillin, Fish
neomycin
penicillin + polymyxin-B Scylla serrata (crab)
penicillin + streptomycin Mugil cephalus (fish)
chloramphenicol Fish
Iloticina Phytoplankton community
* Euglena gracilis,
Mycobacterium phlei
(protozoan)
* Amphibalanus eburneus
(barnacle)
penicillin + streptomycin + chloramphenicol Phytoplankton community
+ neomycin + neomycin + cycloheximide
chloramphenicol + streptomycin + penicillin Cancer magister (crab)
penicillin + streptomycin Ulva (Enteromorpha)
intestinalis (seaweed)
penicillin + streptomycin Hypothesis test with
Cassiopea andromeda
(Cnidaria)
streptomycin + chloramphenicol Phytoplankton community
dihydrostreptomycin + neomycin + penicillin Gonyaulax catenella,
Gonyaulax excavata
(protozoan)
+ amphotericin-B
penicillin + streptomycin + chloramphenicol Dictyosiphon
foeniculaceu s (seaweed)
penicillin, vancomycin, chloramphenicol/ Hypothesis test
vancomycin + penicillin
chloramphenicol Hypothesis test
* Hypothesis test with
Cassiopea andromeda
(Cnidaria)
penicillin + streptomycin Elminius modestus
(barnacle)
chloramphenicol Artemia (artemia)
chloramphenicol Brachionus plicatilis
(rotifers)
ampicillin, carbenicillin, cephaloridine, Seaweed
cephalothin, chloramphenicol,
chlortetracycline, colistin, erythromycin,
gentamicin, kanamycin, lincomicin, nalidixic
acid, neomycin, novobiocin, rifampin,
streptomycin, triple sulfa, tetracycline,
trimethoprim, vancomicin
penicillin + streptomycin + polymyxin B + Seaweed
chloramphenicol
sulfamethazine Hypothesis test with
Arachnoides placenta
(Echinodermata)
* Review (phytoplankton)
penicillin, neomycin, streptomycin Tridacna deresa
(mollusk)
penicillin, kanamycin, erythromycin, Artemia fransciscana
(artemia)
cephalothin, chloramphenicol, ampicillin,
oxacillin, carbenicillin
penicillin, neomycin, gentamycin, kanamycin Micromonas pusilla
(phytoplankton)
* Hypothesis test with
Amphibalanus Amphitrite
(barnacle)
chloramphenicol, oxolinic acid Rotifers
penicillin + dihydrostreptomycin + dextrose Tigriopus californicus
(copepod)
+ chloramphenicol
oxolinic acid, kanamycin, erythromycin, Brachionus plicatilis
(rotifers)
penicillin, streptomycin
penicillin + streptomycin + polymyxin-B + Gymnodinium (protozoan)
chloramphenicol
Penicillin + streptomycin + chloramphenicol Phytoplankton
framycetin + amoxicillin Prorocentrum cordatum
(protozoan)
streptomycin Hypothesis test
* Amphibalanus amphitrite
(barnacle)
* Coscinodiscus wailesii
(phytoplankton)
ampicillin Hypothesis test
* Amphibalanus reticulatus
(barnacle)
chloramphenicol Nodipecten nodosus
(mollusk)
kanamycin, crys-4, streptomycin, Pinctada fucata
(mollusk)
chloramphenicol
penicillin + streptomycin + neomycin Hypothesis test
penicillin + streptomycin + neomycin Hypothesis test
penicillin + streptomycin + neomycin + Hypothesis test
cycloheximide
streptomycin + furaltadone Argopecten purpuratus
(mollusk)
chloramphenicol Argopecten purpuratus
(mollusk)
flumequine, oxytetracycline Brachionus plicatilis
(rotifers)
* Rotifers
chloramphenicol, gentamicin, kanamycin, Alexandrium catenella
(protozoan)
streptomycin, ampicillin, tetracycline
oxytetracycline, oxolinic acid Penaeus monodon (shrimp)
benzylpenicillin + streptomycin Diatom (phytoplankton)
benzylpenicillin + chloramphenicol Hypothesis test
penicillin + streptomycin Phytoplankton
gentamicin + penicillin + streptomycin Pseudo-nitzschia
multiseries (periphyton)
antibiotic + fungicide* Fish
streptomycin Hypothesis test
oxytetracycline Fish
chloramphenicol Isochrysis galbana
(phytoplankton)
penicillin + streptomycin + neomycin Hypothesis test
oxytetracycline Penaeus japonicus
(shrimp)
oxytetracycline Litopenaeus setiferus
(shrimp)
penicillin + streptomycin Alexandrium tamarense
(protozoan)
ampicillin, gentamicin, penicillin, Penaeus monodon (shrimp)
streptomycin, erythromycin,
chlortetracycline, kanamycin
oxytetracycline, amoxicillin, oxolinic acid Hippoglossus
hippoglossus (fish)
ciprofloxacin Lepomis gibbosus (fish)
ciprofloxacin Phytoplankton community
ciprofloxacin Zooplankton community
sulfadiazone, dihydrostreptomycin, tylosin, Raphidocelis
subcapitata, Chlorella
vulgaris (phytoplankton)
norfloxacin, erythromycin, sulfadimethoxine,
cefazolin, ampicillin, trimethoprim,
pyrimethamine, sulfamethoxazole,
oxytetracycline, thiamphenicol
tetracycline + oxytetracycline + doxycycline Phytoplankton community
+ chlortetracycline
tetracycline + oxytetracycline + doxycycline Zooplankton community
+ chlortetracycline
penicillin + streptomycin + polymyxin-B + Cochlodinium
polykrikoides
(protozoan)
chloramphenicol
erythromycin, oxytetracycline, Brachionus calyciflorus
calyciflorus (rotifers)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
erythromycin, oxytetracycline, Thamnocephalus platyurus
(Artemia)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
erythromycin, oxytetracycline, Ceriodaphnia dubia,
Daphnia magna
(cladoceran)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
erythromycin, oxytetracycline, Danio rerio (fish)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
streptomycin + penicillin Hypothesis test
streptomycin + penicillin Hypothesis test
penicillin + streptomycin + neomycin Hypothesis test
several Phytoplankton
chloramphenicol, erythromycin, furaltadone Isochrysis galabana,
Chaetoceros gracilis
(phytoplankton)
tetracycline, oxytetracycline, amoxicillin, Abalone (mollusk)
trimethoprim + sulphonamide, trimethoprim
oxytetracycline Fish
oxytetracycline Penaeus monodon (shrimp)
* Chattonella marina
(phytoplankton)
penicillin + streptomycin Amphibalanus amphitrite,
Fistulobalanus
albicostatus,
Megabalanus rosa
(barnacle)
* Chattonella marina,
Chattonella ovata
(phytoplankton)
penicillin + streptomycin Fistulobalanus
albicostatu s (barnacle)
chloramphenicol, ciprofloxacin, nitrofuratoin Artemia fransciscana
(Artemia)
streptomycin Hypothesis test
streptomycin + kanamycin Hypothesis test
ampicillin, cefuroxina, chloramphenicol, Oreochromis niliticus
(fish)
erythromycin, gentamicin, nitrofurantoin,
norfloxacin, tetracycline, sulfonamides
dihydrostreptomycin, neomycin, Chlorella ellipsoidea,
Isochrysis galbana,
Hetrosigma akashiwo,
chloramphenicol/ neomycin + Cyclotella didymus,
Thalassiosira alleni
(phytoplankton)
dihydrostreptomycin
penicillin + streptomycin Hypothesis test with
Mytilus
galloprovincialis
(mollusk)
penicillin + streptomycin Hypothesis test with
Haliotis iris (mollusk)
nalidixic acid, tetracycline, chloramphenicol, Litopenaeus vannamei
(shrimp)
imipenem, cefoxitin, gentamicin,
ciprofloxacin, rofurantoin, ceftriaxone,
ampicillin, sulphazotrim, trimethoprim
rifampicin Boeckella antiqua
(copepod)
triclosan, triclocarban, roxithromycin, Pseudokirchneriella
subcapitata
(phytoplankton)
clarithromycin, tylosin, tetracycline,
chlortetracycline, norfloxacin,
sulfamethoxazole, ciprofloxacin,
sulfamethazine, trimethoprim
gentamicin Hypothesis test
gentamicin Acartia tonsa (copepod)
penicillin + streptomycin Hypothesis test
chloramphenicol, florfenicol, tianfenicol Chlorella pyrenoidosa,
Isochrysis galbana,
Tetraselmis chui
(phytoplankton)
penicillin + streptomycin/ gentamicin Oxyrrhis marina
(phytoplankton)
penicillin + streptomycin Hypothesis test
* Gadus morhua (fish)
ampicillin, chloramphenicol, kanamycin, Periphyton
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
ampicillin, chloramphenicol, kanamycin, Phytoplankton community
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
ampicillin, chloramphenicol, kanamycin, Zooplankton community
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
ampicillin, chloramphenicol, kanamycin, Macroinvertebrate
community
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
streptomycin, chloramphenicol, kanamycin, Portunus pelagicus
(crab)
co-trimoxazole, erythromycin,
oxytetracycline, ampicillin, nystatin,
gentamicin, penicillin, furazolidone,
ciprofloxacin, rifampicin, neomycin
ciprofloxacin Fragilaria radians
(phytoplankton)
streptomycin Oncomelania hupensis
(mollusk)
imipenem Achnanthidium
minutissimum, Cymbella
affiniformis, Nitzschia
dissipata (phytoplankton
and periphyton)
oxytetracycline, ciprofloxacin Scenedesmus obliquus
(phytoplankton)
chlortetracycline Microcystis aeruginosa,
Scenedesmus obliquus
(phytoplankton)
ciprofloxacin, lincomycin, tylosin Ceratoneis closterium,
Navicula ramosissima
(periphyton)
erythromycin Litopenaeus vannamei
(shrimp)
streptomycin / penicillin, ampicillin, Thraustochytrids
(protozoan)
rifampicin, nalidixic acid, tetracycline,
gentamicin, nystatin
amoxicillin, erythromycin, levofloxacin, Anabaena (cyanobacteria)
norfloxacin, tetracycline
amoxicillin, erythromycin, levofloxacin, Raphidocelis subcapitata
(phytoplankton)
norfloxacin, tetracycline
penicillin + streptomycin Acutodesmus obliquus,
Chlorella kessleri
(phytoplankton)
tylosin Periphyton
penicillin + streptomycin Hypothesis test with
Mytilus unguiculatus
(mollusk)
oxytetracycline + trimethoprim Dolichospermum flosaquae
(cyanobacteria)
oxytetracycline + trimethoprim Raphidocelis subcapitata
(phytoplankton)
oxytetracycline + trimethoprim Daphinea magna
(cladoceran)
enrofloxacin Periphyton
enrofloxacin Phytoplankton community
enrofloxacin Zooplankton community
enrofloxacin Invertebrates
rifampicin, tryptone Mytilus edulis (mollusk)
ciprofloxacin, sulfamethoxazole Periphyton
penicillin + vancomycin/ penicillin + Isochrysis galbana,
Conticribra weissflogii
(phytoplankton)
streptomycin/ neomycin/ penicillin +
streptomycin + chloramphenicol
penicillin + streptomycin/ neomycin/ Temora turbinata
(copepod)
penicillin + chloramphenicol + neomycin +
streptomycin + tetracycline/ penicillin +
streptomycin + chloramphenicol/ penicillin +
vancomycin
penicillin + streptomycin + neomycin/ Acartia tonsa (copepod)
penicillin + streptomycin
streptomycin + ampicillin Limacina helicina
(mollusk)
enrofloxacin, ciprofloxacin Pangasius (fish)
ampicillin + gentamycin + kanamycin + Nannochloropsis sp.,
Cylindrotheca sp.,
Tetraselmis sp.
neomycin + streptomycin Amphikrikos sp.
(phytoplankton)
ampicillin, neomycin, kanamycin, Isochrysis galbana
(phytoplankton)
chloramphenicol, sulphate G418,
streptomycin,
carbencillin
penicillin + streptomycin + neomycin Acartia tonsa (copepod)
Antimicrobials used Author(s)
penicillin Ithaca & Mahmoud (1944)
* Morgan (1946)
penicillin Williams & Plastridge
(1946)
penicillin Seaman (1947)
* Fish (1950)
* Epps (1950)
penicillin, dihydrostreptomycin Goodwin (1950)
aureomycin + oxytetracycline hydrochloride Speck et al. (1951)
+ penicillin
streptomycin Ca[Cl.sub.2] + penicillin Spencer (1952)
penicillin Spencer (1952)
penicillin + streptomycin Pappas & Hoffman (1952)
nystatin Donovick et al. (1955)
penicillin + streptomycin Oppenheimer (1955)
penicillin + streptomycin Walne (1956)
penicillin Costlow & Bookhout
(1957)
aureomycin Velankar (1958)
penicillin + streptomycin Walne (1958)
streptomycin Marshall & Orr (1958)
terramycin, streptomycin, polymyxin-B, Galloway & Krauss (1959)
tetracycline, penicillin, bacitracin,
chloromycetin and gramicidin
penicillin Palincsar (1959)
streptomycin Tuker (1959)
aureomycin, chloramphenicol, tetracycline, Miller & Johnson (1959)
streptomycin, neomycin, erytromycin,
novobiocin, vancomycin, penicillin,
trypaflavin, filipin
penicillin + streptomycin Fulton (1959)
chlortetracycline + chloramphenicol + Fell et al. (1960)
streptomycin
bicyclohexylamine Claybrook & Eakin (1960)
penicillin + streptomycin Dougherty et al. (1960)
penicillin Boalch (1961)
nystatin Lampen & Arnow (1961)
* Tchan & Gould (1961)
* Kinsky (1961)
chlortetracycline + citric acid Suehiro & Tomiyase
(1962)
penicillin + streptomycin/ chloramphenicol Guillard (1959)
penicillin + dihydrostreptomycin Guillard & Ryther (1962)
penicillin + chloramphenicol + neomycin + Provasoli & Gold (1962)
polymyxin-B + dihydrostreptomicin +
tetracycline + candicidin
streptomycin, penicilin Conover (1962)
penicillin + streptomycin Walne (1963)
amphotericin-B + streptomycin Ghosh & Ghosh (1963)
penicillin + streptomycin Fries (1963)
penicillin + chloramphenicol + neomycin + Provasoli & McLaughlin
(1963)
polymyxin B
dihydrostreptomycin + streptomycin Hidu & Tubiash (1963)
polymyxin-B + neomycin Soli (1964)
chlortetracycline + citric acid Suehiro & Tomiyase
(1964)
penicillin + streptomycin Fuller et al. (1964)
penicillin + streptomycin Stickney (1964)
penicillin + streptomycin + chloramphenicol Keck (1964)
penicillin + streptomycin Bayne (1965)
penicillin + streptomycin + chloramphenicol Antia & Kalmakoff (1965)
+ Tween-80
cycloheximide Ray (1965)
penicillin + streptomycin Neunes & Pongolini
(1965)
streptomycin, penicillin Conover (1966)
penicillin + streptomycin Borojevic (1966)
penicillin + dihydrostreptomycin Cook & Murphy (1966)
cycloheximide, oxytetracycline, Ray (1966)
chlortetracycline, tetracycline
penicillin + streptomycin + chloramphenicol Millar & Scott (1967)
sulfamethazine Calabrese & Davis (1967)
streptomycin, penicillin Conover (1967)
tetracycline, streptomycin, penicillin Stephens (1967)
chloramphenicol + chlortetracycline + Meyers et al. (1967)
streptomycin
chloramphenicol + streptomycin / penicillin Droop (1967)
+ streptomycin + neomycin +
chloramphenicol
penicillin + neomycin + nystatin Green et al. (1967)
penicillin + streptomycin Mullin & Brooks (1967)
penicillin + dihydrostreptomycin + nystatin Khouw et al. (1968)
chloramphenicol Ahearn et al. (1968)
gentamicin Ahearn et al. (1968)
penicillin + streptomycin Gold (1968)
penicillin + streptomycin Gold (1969)
neomycin + streptomycin Minaur (1969)
* Muller (1969)
penicillin + streptomycin Viglierchio et al.
(1969)
penicillin + streptomycin Berglund (1969)
chloramphenicol + novobiocin Muller & Lee (1969)
spiramycin, ristocetin, sulfamerazine, triple Berland & Maestrini
(1969)
sulpha, vancomycin, penicillin, streptomycin
penicillin + streptomycin Pilkington & Fretter
(1970)
penicillin + carbenicillin + kanamycin + Shephard (1970)
vancomycin
novobiocin + erythromycin, novobiocin + Lee et al. (1970)
colimycin + nystatin, novobiocin + colimycin
+ fungizone
penicillin + streptomycin Tighe-Ford et al.
(1970)
penicillin Nassogne (1970)
penicillin + streptomycin Walne (1970)
chloramphenicol Seshadri & Sieburth
(1971)
penicillin Roberts (1972)
penicillin + streptomycin + chloromycetin McCammon (1972)
dihydrostreptomycin, binotal Hoppe (1972)
several D'Agostino (1972)
penicillin + gentamicin + streptomycin Hoshaw & Rosowski
(1973)
penicillin + chloramphenicol + neomycin + Jones et al. (1973)
penicillin + tetracycline + chloramphenicol +
aureomycin + ceporin + neomycin
colimycin, geopen + carbenicillin, penicillin, Struhsaker et al. (1973)
penicillin + ampicillin, keflin + cephalothin,
aerosporin
erythromycin, carbenicillin, penicillin, Struhsaker et al. (1973)
ampicillin, cephalothin, nitrofurantoin,
sulfadiazine
chloramphenicol + colimycin Lee (1974)
colimycin, streptomycin, penicillin, Struhsaker et al. (1974)
neomycin
penicillin + polymyxin-B Brick (1974)
penicillin + streptomycin Nash et al. (1974)
chloramphenicol Struhsaker et al. (1975)
Iloticina Sheath (1975)
* Ebringer et al. (1976)
* Landau & D'Agostino
(1977)
penicillin + streptomycin + chloramphenicol Vieira (1977)
+ neomycin + neomycin + cycloheximide
chloramphenicol + streptomycin + penicillin Fisher & Nelson (1978)
penicillin + streptomycin Millner et al. (1979)
penicillin + streptomycin Neumann (1979)
streptomycin + chloramphenicol Tipper & Wright (1979)
dihydrostreptomycin + neomycin + penicillin Divan & Schnoes (1982)
+ amphotericin-B
penicillin + streptomycin + chloramphenicol Saga & Sakai (1982)
penicillin, vancomycin, chloramphenicol/ Sherr et al. (1986)
vancomycin + penicillin
chloramphenicol Wheeler & Kirchmann
(1986)
* Fitt et al. (1987)
penicillin + streptomycin Harms (1987)
chloramphenicol Benavente & Gatesoupe
(1988)
chloramphenicol Benavente & Gatesoupe
(1988)
ampicillin, carbenicillin, cephaloridine, Bradley et al. (1988)
cephalothin, chloramphenicol,
chlortetracycline, colistin, erythromycin,
gentamicin, kanamycin, lincomicin, nalidixic
acid, neomycin, novobiocin, rifampin,
streptomycin, triple sulfa, tetracycline,
trimethoprim, vancomicin
penicillin + streptomycin + polymyxin B + Tatewaki (1989)
chloramphenicol
sulfamethazine Chen & Run (1980)
* McCracken (1989)
penicillin, neomycin, streptomycin Fitt et al. (1992)
penicillin, kanamycin, erythromycin, Rosowski et al. (1992)
cephalothin, chloramphenicol, ampicillin,
oxacillin, carbenicillin
penicillin, neomycin, gentamycin, kanamycin Cottrel & Suttle (1993)
* Avelin Mary et al.
(1993)
chloramphenicol, oxolinic acid Hernandez-Cruz et al.
(1994)
penicillin + dihydrostreptomycin + dextrose Shaw et al. (1994)
+ chloramphenicol
oxolinic acid, kanamycin, erythromycin, Munro et al. (1995)
penicillin, streptomycin
penicillin + streptomycin + polymyxin-B + Hasui et al. (1995)
chloramphenicol
Penicillin + streptomycin + chloramphenicol Gonzalez et al. (1995)
framycetin + amoxicillin Grzebyk et al. (1997)
streptomycin Maurin et al. (1997)
* Thomason et al. (1998)
* Nagai et al. (1998)
ampicillin Ringelberg & Van Gool
(1998)
* Lee et al. (1999)
chloramphenicol Bem (1999)
kanamycin, crys-4, streptomycin, Dharmaraj&
Shahmugasundaram
chloramphenicol (1999)
penicillin + streptomycin + neomycin Middelburg &
Nieuwenhuize (2000a)
penicillin + streptomycin + neomycin Middelburg &
Nieuwenhuize, 2000b
penicillin + streptomycin + neomycin + DeLorenzo et al. (2001)
cycloheximide
streptomycin + furaltadone Riquelme et al. (2001)
chloramphenicol Uriarte et al. (2001)
flumequine, oxytetracycline Goksan & Gokpinar (2001)
* Dhert et al. (2001)
chloramphenicol, gentamicin, kanamycin, Codova et al. (2002)
streptomycin, ampicillin, tetracycline
oxytetracycline, oxolinic acid Tendencia & Pena (2002)
benzylpenicillin + streptomycin Wolfstein et al. (2002)
benzylpenicillin + chloramphenicol Bidle et al. (2003)
penicillin + streptomycin Tavares & Rocha (2003)
gentamicin + penicillin + streptomycin Kobayashi et al. (2003)
antibiotic + fungicide* Saborido-Rey et al.
(2003)
streptomycin Tungaraza et al. (2003)
oxytetracycline Bruun et al. (2003)
chloramphenicol Subhash et al. (2004)
penicillin + streptomycin + neomycin Veuger et al. (2004)
oxytetracycline Uno (2004)
oxytetracycline Reed et al. (2004)
penicillin + streptomycin Wang et al. (2004)
ampicillin, gentamicin, penicillin, Vaseeharan et al. (2004)
streptomycin, erythromycin,
chlortetracycline, kanamycin
oxytetracycline, amoxicillin, oxolinic acid Verner-Jaffreys et al.
(2004)
ciprofloxacin Richards et al. (2004)
ciprofloxacin Richards et al. (2004)
ciprofloxacin Richards et al. (2004)
sulfadiazone, dihydrostreptomycin, tylosin, Eguchi et al. (2004)
norfloxacin, erythromycin, sulfadimethoxine,
cefazolin, ampicillin, trimethoprim,
pyrimethamine, sulfamethoxazole,
oxytetracycline, thiamphenicol
tetracycline + oxytetracycline + doxycycline Wilson et al. (2004)
+ chlortetracycline
tetracycline + oxytetracycline + doxycycline Wilson et al. (2004)
+ chlortetracycline
penicillin + streptomycin + polymyxin-B + Cho & Costas (2004)
chloramphenicol
erythromycin, oxytetracycline, Isidori et al. (2005)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
erythromycin, oxytetracycline, Isidori et al. (2005)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
erythromycin, oxytetracycline, Isidori et al. (2005)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
erythromycin, oxytetracycline, Isidori et al. (2005)
sulfamethoxazole, ofloxacin, lincomycin,
clarithromycin
streptomycin + penicillin Tang et al. (2006a)
streptomycin + penicillin Tang et al. (2006b)
penicillin + streptomycin + neomycin Cozzi & Cantoni (2006)
several Lourenco (2006)
chloramphenicol, erythromycin, furaltadone Campa-Cordova et al.
(2006)
tetracycline, oxytetracycline, amoxicillin, Handlinger et al. (2006)
trimethoprim + sulphonamide, trimethoprim
oxytetracycline Pereira Jr. et al.
(2006)
oxytetracycline Uno et al. (2006)
* Kim et al. (2006)
penicillin + streptomycin Yoshimura et al. (2006)
* Kim et al. (2007)
penicillin + streptomycin Chen et al. (2007)
chloramphenicol, ciprofloxacin, nitrofuratoin Castro-Mejia et al.
(2007)
streptomycin Fouilland et al. (2007)
streptomycin + kanamycin Hamdan & Jonas (2007)
ampicillin, cefuroxina, chloramphenicol, Carneiro et al. (2007)
erythromycin, gentamicin, nitrofurantoin,
norfloxacin, tetracycline, sulfonamides
dihydrostreptomycin, neomycin, Youn & Hur (2007)
chloramphenicol/ neomycin +
dihydrostreptomycin
penicillin + streptomycin Bao et al. (2007)
penicillin + streptomycin Roberts et al. (2007)
nalidixic acid, tetracycline, chloramphenicol, Costa et al. (2008)
imipenem, cefoxitin, gentamicin,
ciprofloxacin, rofurantoin, ceftriaxone,
ampicillin, sulphazotrim, trimethoprim
rifampicin Garcia et al. (2008)
triclosan, triclocarban, roxithromycin, Yang et al. (2008)
clarithromycin, tylosin, tetracycline,
chlortetracycline, norfloxacin,
sulfamethoxazole, ciprofloxacin,
sulfamethazine, trimethoprim
gentamicin Tartarotti & Torres
(2009)
gentamicin Tartarotti & Torres
(2009)
penicillin + streptomycin Pringault et al. (2009)
chloramphenicol, florfenicol, tianfenicol Lai et al. (2009)
penicillin + streptomycin/ gentamicin Lowe et al. (2011)
penicillin + streptomycin Trotted et al. (2011)
* Forberg et al. (2011)
ampicillin, chloramphenicol, kanamycin, Suga et al. (2011)
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
ampicillin, chloramphenicol, kanamycin, Suga et al. (2011)
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
ampicillin, chloramphenicol, kanamycin, Suga et al. (2011)
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
ampicillin, chloramphenicol, kanamycin, Suga et al. (2011)
nalidixic acid, streptomycin/ ampicillin +
kanamycin + nalidixic acid + streptomycin
streptomycin, chloramphenicol, kanamycin, Talpur et al. (2011)
co-trimoxazole, erythromycin,
oxytetracycline, ampicillin, nystatin,
gentamicin, penicillin, furazolidone,
ciprofloxacin, rifampicin, neomycin
ciprofloxacin Shishlyannikov et al.
(2011)
streptomycin Aina et al. (2012)
imipenem Windler et al. (2012)
oxytetracycline, ciprofloxacin Zhang et al. (2012)
chlortetracycline Guo & Chen (2012)
ciprofloxacin, lincomycin, tylosin Hagenbuch & Pinckney
(2012)
erythromycin Rego et al. (2012)
streptomycin / penicillin, ampicillin, Wilkens & Maas (2012)
rifampicin, nalidixic acid, tetracycline,
gentamicin, nystatin
amoxicillin, erythromycin, levofloxacin, Gonzalez-Pleiter et al.
(2013)
norfloxacin, tetracycline
amoxicillin, erythromycin, levofloxacin, Gonzalez-Pleiter et al.
(2013)
norfloxacin, tetracycline
penicillin + streptomycin Stemmler (2013)
tylosin Pinckney et al. (2013)
penicillin + streptomycin Yang et al. (2013)
oxytetracycline + trimethoprim Kolar et al. (2014)
oxytetracycline + trimethoprim Kolar et al. (2014)
oxytetracycline + trimethoprim Kolar et al. (2014)
enrofloxacin Rico et al. (2014)
enrofloxacin Rico et al. (2014)
enrofloxacin Rico et al. (2014)
enrofloxacin Rico et al. (2014)
rifampicin, tryptone Eggermont et al. (2014)
ciprofloxacin, sulfamethoxazole Johansson et al. (2014)
penicillin + vancomycin/ penicillin + Agostini (2014)
streptomycin/ neomycin/ penicillin +
streptomycin + chloramphenicol
penicillin + streptomycin/ neomycin/ Agostini (2014)
penicillin + chloramphenicol + neomycin +
streptomycin + tetracycline/ penicillin +
streptomycin + chloramphenicol/ penicillin +
vancomycin
penicillin + streptomycin + neomycin/ Agostini (2014)
penicillin + streptomycin
streptomycin + ampicillin Howes et al. (2014)
enrofloxacin, ciprofloxacin Andrieu et al. (2015)
ampicillin + gentamycin + kanamycin + Han et al. (2016)
neomycin + streptomycin
ampicillin, neomycin, kanamycin, Molina-Cardenas et al.
(2016)
chloramphenicol, sulphate G418,
streptomycin,
carbencillin
penicillin + streptomycin + neomycin Agostini et al. (2016)
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