Parasites as biological tags for stock discrimination in marine fish from South American Atlantic waters

The use of parasites as biological tags in population studies of marine fish in the south-western Atlantic has proved to be a successful tool for discriminating stocks for all species to which it has been applied, namely: Scomber japonicus, Engraulis anchoita, Merluccius hubbsi and Cynoscion guatucupa, the latter studied on a broader geographic scale, including samples from Uruguayan and Brazilian waters. The distribution patterns of marine parasites are determined mainly by temperature-salinity profiles and by their association with specific masses of water. Analyses of distribution patterns of some parasite species in relation to gradients in environmental (oceanographic) conditions showed that latitudinal gradients in parasite distribution are common in the study area, and are probably directly related to water temperature. Indeed, temperature, which is a good predictor of latitudinal gradients of richness and diversity of species, shows a latitudinal pattern in south-western Atlantic coasts, decreasing southwards, due to the influence of subtropical and subantarctic marine currents flowing along the edge of the continental slope. This pattern also determines the distribution of zooplankton, with a characteristic specific composition in different water masses. The gradient in the distribution of parasites determines differential compositions of their communities at different latitudes, which makes possible the identification of different stocks of their fish hosts. Other features of the host-parasite systems contributing to the success of the parasitological method are: (1) parasites identified as good biological tags (i.e. anisakids) are widely distributed in the local fauna; (2) many of these species show low specificity and use paratenic hosts; and (3) the structure of parasite communities are, to a certain degree, predictable in time and space.     

Community ecology of the parasites of adult spot, Leiostomus xanthurus, and Atlantic croaker, Micropogonias undulatus (Sciaenidae) in the Cape Hatteras region

Twenty-three species of metazoan parasites were recorded from adult spot and 26 from adult croaker. Of the 33 parasitic species found, 17 occurred in both spot and croaker. No significant differences in intensity of parasites occurred between sexes of either spot or croaker. All of the parasites had over-dispersed, or clumped, distributions among hosts. Adult spot and croaker collected offshore had much greater species-richness, diversity, and total number of individual parasites than juvenile fishes collected in adjoining estuaries during another study. The juvenile spot and croaker had less time to acquire parasites and inhabited less diverse and more confined habitats in inshore estuaries, which resulted in less diverse parasite communities than offshore fishes. The number of species and diversity of parasites in adult fish was greater in croaker than spot. However, when only gastrointestinal helminths were considered, spot had greater species-richness as well as greater numbers of individual helminths, suggesting that they had a more diverse diet and that they fed on more infected intermediate hosts than croaker. In both adult spot and croaker the mean number of parasitic species was greater than those of freshwater fishes and fewer than those for birds and mammals. The total number of individual parasites was similar to that of freshwater fishes. The opportunistic diet and the migratory habits of both spot and croaker contribute to their diverse parasite faunas. Comparison of adult spot and croaker parasite faunas collected offshore indicated that their respective parasite component communities were distinct and that similar parasite infracommunity variability existed in both hosts and that their communities were not ‘random’ samples, but restricted subsets of the compound community. Although the parasite dominance hierarchy in adults of both species varied slightly between areas and seasons sampled, there appeared to be a predictable dominant species that was accompanied by subordinate, less predictable species. However, the variability in both relative intensities and presence-absence of parasites within communities resulting from their diverse diets make them less predictable than those of other vertebrates with less diverse diets such as the lesser scaup duck and more like those of other marine fishes.     

Community ecology of the metazoan parasites of pink cusk-eel,Genypterus brasiliensis (Osteichthyes: Ophidiidae), from the coastal zone of the State of Rio de Janeiro,Brazil

Fifty-five specimens of pink cusk-eel, Genypterus brasiliensis Regan, 1903 (Osteichthyes: Ophidiidae) collected from the coastal zone of the State of Rio de Janeiro, Brazil (approx. 21-23 degrees S, 41-45 degrees W), from September 2000 to January 2001, were necropsied to study their parasites. All fish were parasitized by one or more metazoan. Fourteen species of parasites were collected. G. brasiliensis is a new host record for nine parasite species. The larval stages of cestodes and the nematodes were the majority of the parasite specimens collected, with 38.4% and 36.5%, respectively. Cucullanus genypteri was the dominant species with highest prevalence and/or abundance. The parasites of G. brasiliensis showed the typical overdispersed pattern of distribution. Six parasite species showed correlation between the host's total body length and prevalence and abundance. Host sex did not influence prevalence and parasite abundance of any parasite species. The mean diversity in the infracommunities of G. brasiliensis was H= 0.364 +/- 0.103, with correlation with the host's total length and without differences in relation to sex of the host. One pair of adult endoparasites (C. genypteri and A. brasiliensis) showed positive covariations between their abundances. Negative association or covariation was not found. Differences between the qualitative and quantitative aspects of the parasite community of G. brasiliensis from Rio de Janeiro and Argentina suggest the existence of two population stocks of pink cusk-eel in the South America Atlantic Ocean.     

Native fish avoid parasite spillback from multiple exotic hosts: consequences of host density and parasite competency

Disease-mediated impacts of exotic species on their native counterparts are often ignored when parasite-free individuals are translocated. However, native parasites are frequently acquired by exotic species, thus providing a mechanism through which native host-parasite dynamics may be altered. In Argentina, multiple exotic salmonids are host to the native fish acanthocephalan parasite Acanthocephalus tumescens. Field evidence suggests that rainbow trout, Oncorhynchus mykiss, may be a major contributor to the native parasite’s population. We used a combination of experimental infections (cystacanth—juvenile worm transmission from amphipod to fish; post-cyclic—adult worm transmission between definitive fish hosts) and dynamic population modelling to determine the extent to which exotic salmonid hosts may alter A. tumescens infections in native freshwater fish. Experimental cystacanth infections demonstrated that although A. tumescens establishes equally well in native and exotic hosts, parasite growth and maturity is superior in exotic O. mykiss. Experimental post-cyclic infections also showed greater establishment success of A. tumescens in O. mykiss, though post-cyclic transmission did not result in greater parasite size or maturity. Dynamic population modelling, however, suggested that exotic salmonids may have a very limited influence on the A. tumescens population overall, due to the majority of A. tumescens individuals being maintained by more abundant native hosts. This research highlights the importance of considering both a host’s relative density and its competency for parasites when evaluating whether exotic species can modify native host-parasite dynamics.     

Nested assemblages resulting from host size variation: the case of endoparasite communities in fish hosts

Nested species subsets are a common pattern in many types of communities found in insular or fragmented habitats. Nestedness occurs in some communities of ectoparasites of fish, as does the exact opposite departure from random assembly, anti-nestedness. Here, we looked for nested and anti-nested patterns in the species composition of communities of internal parasites of 23 fish populations from two localities in Finland. We also compared various community parameters of nested and anti-nested assemblages of parasites, and determined whether nestedness may result simply from a size-related accumulation of parasite species by feeding fish hosts. Nested parasite communities were characterised by higher prevalence (proportion of infected fish) and intensities of infection (number of parasites per fish) than anti-nested communities; the two types of non-random communities did not differ with respect to parasite species richness, however. In addition, the correlation between fish size and the number of parasite species harboured by individual fish was much stronger in nested assemblages than in anti-nested ones, where it was often nil. These results were shown not to be artefacts of sampling effort or host phylogeny. They apply to both assemblages of adult and larval parasites, which were treated separately. Since species of larval parasites are extremely unlikely to interact with one another in fish hosts, the establishment of nestedness appears independent of the potential action of interspecific interactions. The species composition of these parasite communities is not determined from within the community, but rather by the extrinsic influence of host feeding rates and how they amplify differences among parasite species in probabilities of colonisation or extinction. Nested patterns occur in parasite communities whose fish hosts accumulate parasites in a predictable fashion proportional to their size, whereas anti-nested communities occur in parasite communities whose fish hosts do not, possibly because of dietary specialisation preventing them from sampling the entire pool of parasite species available locally. Thus, nestedness in parasite communities may result from processes somewhat different from those generating nested patterns in free-living communities.     

Body size,trophic level,and the use of fish as transmission routes by parasites

Within food webs, trophically transmitted helminth parasites use predator–prey links for their own transfer from intermediate prey hosts, in which they occur as larval or juvenile stages, to predatory definitive hosts, in which they reach maturity. In large taxa that can be used as intermediate and/or definitive hosts, such as fish, a host species’ position within a trophic network should determine whether its parasite fauna consists mostly of adult or larval helminths, since vulnerability to predation determines an animal’s role in predator–prey links. Using a large database on the helminth parasites of 303 fish species, we tested whether the proportion of parasite species in a host that occur as larval or juvenile stages is best explained by their trophic level or by their body size. Independent of fish phylogeny or habitat, only fish body length emerged as a significant predictor of the proportion of parasites in a host that occur as larval stages from our multivariate analyses. On average, the proportion of larval helminth taxa in fish shorter than 20 cm was twice as high as that for fish over 100 cm in length. This is consistent with the prediction that small fishes, being more vulnerable to predation, make better hosts for larval parasites. However, trophic level and body length are strongly correlated among fish species, and they may have separate though confounded effects on the parasite fauna exploiting a given species. Helminths show varying levels of host specificity toward their intermediate host when the latter is the downstream host involved in trophic transmission toward an upstream definitive host. Given this broad physiological compatibility of many helminths with fish hosts, our results indicate that fish body length, as a proxy for vulnerability to predators, is a better predictor of their use by helminth larvae than their trophic level based on diet content.     

Parasites as biological tags for stock discrimination of the Brazilian flathead Percophis brasiliensis in the south-west Atlantic

Three stocks of the Brazilian flathead Percophis brasiliensis were identified on the coast of Argentina and Uruguay using parasites as biological tags. A total of 177 fish were examined and 23 parasite species were found. Fish were caught in four zones: north of the Argentine–Uruguayan Common Fishing Zone (34°30′–36°30′ S; 53°30′–56°00′ W), south of the Argentine–Uruguayan Common Fishing Zone (38°08′ S 57°32′ W), El Rincón zone (39–41° S; 60–62° W) and San Matías Gulf (41°40′–42°10′ S; 63°50′–65°00′ W). Discriminant analyses allowed the identification of three discrete stocks in the four zones (86·44% of classified samples were correctly identified), with P. brasiliensis from both north and south of the Argentine–Uruguayan Common Fishing Zone clumping together, as a single stock. Some species were important in discriminating among groups, Anisakis simplex was related to southern areas, while Grillotia sp., Corynosoma australe and Hysterothylacium sp. were important in determining the position of fish from the Argentine–Uruguayan Common Fishing Zone. These results were corroborated by comparing parasite prevalence and abundance among zones. The main differences were observed in those comparisons involving fish from the San Matías Gulf. Fish from the Argentine–Uruguayan Common Fishing Zone were characterized by higher infections of Grillotia sp., C. australe, Corynosoma cetaceum and Hysterothylacium sp., while the samples from El Rincón and San Matías Gulf showed higher infections of A. simplex. Samples from San Matías Gulf were characterized by lower levels of parasitism for all other species. Differences in environmental factors and their influence on the distribution of zooplankton and other hosts in the food web may be differentially shaping the parasite community structure in each zone, resulting in identifiable stocks of the P. brasiliensis. The present study confirmed the existence of regional biological tags that delineated fish assemblages.     

Host sex and ectoparasites choice: preference for, and higher survival on female hosts

1. Sex differences in levels of parasite infection are a common rule in a wide range of mammals, with males usually more susceptible than females. Sex-specific exposure to parasites, e.g. mediated through distinct modes of social aggregation between and within genders, as well as negative relationships between androgen levels and immune defences are thought to play a major role in this pattern. 2. Reproductive female bats live in close association within clusters at maternity roosts, whereas nonbreeding females and males generally occupy solitary roosts. Bats represent therefore an ideal model to study the consequences of sex-specific social and spatial aggregation on parasites' infection strategies. 3. We first compared prevalence and parasite intensities in a host-parasite system comprising closely related species of ectoparasitic mites (Spinturnix spp.) and their hosts, five European bat species. We then compared the level of parasitism between juvenile males and females in mixed colonies of greater and lesser mouse-eared bats Myotis myotis and M. blythii. Prevalence was higher in adult females than in adult males stemming from colonial aggregations in all five studied species. Parasite intensity was significantly higher in females in three of the five species studied. No difference in prevalence and mite numbers was found between male and female juveniles in colonial roosts. 4. To assess whether observed sex-biased parasitism results from differences in host exposure only, or, alternatively, from an active, selected choice made by the parasite, we performed lab experiments on short-term preferences and long-term survival of parasites on male and female Myotis daubentoni. When confronted with adult males and females, parasites preferentially selected female hosts, whereas no choice differences were observed between adult females and subadult males. Finally, we found significantly higher parasite survival on adult females compared with adult males. 5. Our study shows that social and spatial aggregation favours sex-biased parasitism that could be a mere consequence of an active and adaptive parasite choice for the more profitable host.     

Vulnerability and diet breadth predict larval and adult parasite diversity in fish of the Bothnian Bay

Recent studies of aquatic food webs show that parasite diversity is concentrated in nodes that likely favour transmission. Various aspects of parasite diversity have been observed to be correlated with the trophic level, size, diet breadth, and vulnerability to predation of hosts. However, no study has attempted to distinguish among all four correlates, which may have differential importance for trophically transmitted parasites occurring as larvae or adults. We searched for factors that best predict the diversity of larval and adult endoparasites in 4105 fish in 25 species studied over a three-year period in the Bothnian Bay, Finland. Local predator–prey relationships were determined from stomach contents, parasites, and published data in 8,229 fish in 31 species and in seals and piscivorous birds. Fish that consumed more species of prey had more diverse trophically transmitted adult parasites. Larval parasite diversity increased with the diversity of both prey and predators, but increases in predator diversity had a greater effect. Prey diversity was more strongly associated with the diversity of adult parasites than with that of larvae. The proportion of parasite species present as larvae in a host species was correlated with the diversity of its predators. There was a notable lack of association with the diversity of any parasite guild and fish length, trophic level, or trophic category. Thus, diversity is associated with different nodal properties in larval and adult parasites, and association strengths also differ, strongly reflecting the life cycles of parasites and the food chains they follow to complete transmission.     

Metazoan parasites as biological tags for stock discrimination of whitemouth croaker Micropogonias furnieri

Examination of 248 adult specimens of whitemouth croaker Micropogonias furnieri from five localities along the Brazilian coast revealed 8735 parasites belonging to 41 metazoan species. Samples from Ceará to Bahia and Rio de Janeiro to Santa Catarina showed a high level of correct assignation (92 and 87%, respectively) and cross assignation (i.e. almost all specimens misidentified in Ceará were assigned to Bahia and almost all specimens misidentified in Bahia were classified as Ceará), so samples were pooled in the northern and south‐eastern samples, and Rio Grande do Sul was considered a southern area. Eight parasite species were characteristic of the northern localities, five species were found just in the area associated with south‐eastern localities and two species were characteristic of the southern area providing first evidence of stock discreteness. The multivariate discriminant analysis successfully discriminated three groups of localities associated with three stocks of M. furnieri in Brazil: a northern stock associated with Ceará and Bahia, a south‐eastern stock related to Rio de Janeiro and Santa Catarina and a southern stock in the area of Rio Grande do Sul, which could be considered as the northern limit of the stock associated with the Common Fishing Zone of Uruguay and Argentina.     

Seasonal stability and spatial variability of parasites in Brazilian sandperch Pinguipes brasilianus from the Northern Argentine Sea: evidence for stock discrimination

The use of parasites as biological tags allowed the identification of two stocks of Brazilian sandperch Pinguipes brasilianus , in the Bonaerense region of the Argentine Sea. A total of 156 adult specimens of P. brasilianus were examined for parasites. Temporal variability in parasite burdens was assessed from fish caught seasonally in coastal waters of two zones, south Bonaerense (during autumn and winter) and north Bonaerense (during summer). Additional data from a previous study, comprising P. brasilianus caught during spring in these two zones, as well as in two populations from north Patagonian gulfs were used for comparative analyses of spatial variability. A total of 14 193 metazoan parasites belonging to 19 species were found. Comparisons of seasonal variability in pooled samples and within each locality showed that locality effects exceeded seasonal ones, suggesting the possible existence of two discrete stocks in the Bonaerense region. These findings were strongly supported by discriminant analyses and comparisons of prevalence and abundance between zones, after pooling seasonal samples within each zone. Further evidence of the discreteness of both stocks was assessed by inclusion of samples from Patagonian gulfs in the discriminant analysis, confirming that their differences were at a inter-population level. The parasite species that contributed most to the separation of the samples were generally those identified as biological markers in previous studies. Differing oceanographic conditions are discussed as potential causes of inter-population variation of parasite burdens.     

Effects of host migration, diversity and aquaculture on sea lice threats to Pacific salmon populations

Animal migrations can affect disease dynamics. One consequence of migration common to marine fish and invertebrates is migratory allopatry-a period of spatial separation between adult and juvenile hosts, which is caused by host migration and which prevents parasite transmission from adult to juvenile hosts. We studied this characteristic for sea lice (Lepeophtheirus salmonis and Caligus clemensi) and pink salmon (Oncorhynchus gorbuscha) from one of the Canada's largest salmon stocks. Migratory allopatry protects juvenile salmon from L. salmonis for two to three months of early marine life (2-3% prevalence). In contrast, host diversity facilitates access for C. clemensi to juvenile salmon (8-20% prevalence) but infections appear ephemeral. Aquaculture can augment host abundance and diversity and increase parasite exposure of wild juvenile fish. An empirically parametrized model shows high sensitivity of salmon populations to increased L. salmonis exposure, predicting population collapse at one to five motile L. salmonis per juvenile pink salmon. These results characterize parasite threats of salmon aquaculture to wild salmon populations and show how host migration and diversity are important factors affecting parasite transmission in the oceans.     

Population dynamics and community analysis of the parasite fauna of juvenile spot, Leiostomus xanthurus (Lacepede), and Atlantic croaker, Micropogonias undulatus (Linnaeus), Sciaenidae) in two estuaries along the middle Atlantic coast of the United States

The parasite communities of juvenile spot, Leiostomus xanthurus Lacepede, and Atlantic croaker, Micropogonias undulatus (Linnaeus), changed with size, season. and geographical area. A total of 21 parasitic species occurred in juvenile spot and 19 occurred in juvenile croaker from Chesapeake Bay and Pamlico Sound. More parasitic species were acquired as juveniles grew, diversified their diets, and consumed larger numbers of intermediate hosts. They were also exposed to infective larvae of parasites with direct lifecycles over long periods of time. Equibility and, thus, diversity were depressed because of large numbers of Diplomonorchis /eiostomi Hopkins, I941 that dominated the parasite communities of both species. Although spot and croaker from both estuaries shared eight and six parasites, respectively, many of these non-specific parasites (generalists) were more common in both spot and croaker from one estuary than from the other. All species occurring in both hosts have indirect life cycles suggesting that the availability of certain intermediate hosts as prey was an important determinant of infection. Estuary of residence was clearly as important as host species identity in determining parasite community structure.     

Parasitology of the English Sole, Parophrys vetulus Girard in Oregon, U.S.A.

A total of 877 juvenile English sole ( Parophrys vetulus Girard) from the Yaquina Bay estuary and742 juvenileandadultsole from the Pacific Ocean off Oregon were examined forparasites. Fifteen species of parasites were found in juvenile English sole on the estuarine nursery ground. Differences in the prevalence and intensity of parasite infection between size classes of juvenile sole and between sole occupying the upper and lower estuary were determined. An additional 14 parasite species were found in offshore English sole, bringing the total observed in all fish to 29 species. Parasites acquired only in the estuary included the microsporidan Glugea stephani , the acanthocephalan Echinorhynchus lageniformis , and the nematode Philometra americana . Those acquired only in offshore areas included the trematodes Otodistomum veliporum and Zoogonus dextrocirrus , the leech Oceanobdella sp. and three species of copepods. An attempt to use parasite data to indicate the presence of distinct English sole stocks along the Oregon coast was inconclusive.     

Determinants of host-specificity in parasites of freshwater fishes.

Factors responsible for interspecific variability in host-specificity were investigated within 15 genera (including 176 species) of metazoan parasites found in Canadian freshwater fish. For each species in a genus, the parasite's number of known hosts was determined from published host-parasite records. The effects of the total number and mean size of potential hosts (i.e. all fish species belonging to the family or families that include a parasite's known hosts) on number of hosts of congeneric species were evaluated using multiple regressions. Since parasite species that have been recorded often tend to have greater numbers of known hosts than do seldom-recorded parasites, it was necessary to control for the confounding effect of study intensity. In all parasite genera, whether from highly specific taxa such as monogeneans or from less host-specific ones, there was a positive relationship between the number of potential hosts and the number of known hosts. However, no consistent relationships were observed between the mean size of potential hosts and number of known hosts. These results suggest that the availability of suitable host species may have been a key factor limiting the colonization of new hosts by fish parasites.     

Parasite fauna of bream Abramis brama and roach Rutilus rutilus from a man-made waterway and a freshwater habitat in northern Germany

Fifty specimens each of bream Abramis brama and roach Rutilus rutilus were examined for metazoan parasite fauna and trichodinid ciliates; 25 specimens of each species were collected from the Kiel Canal, a man-made waterway, and a nearby freshwater lake, the Dieksee. This is the first detailed parasitological examination of A. brama and R. rutilus at these locations: 30 parasite species were found, comprising 4 protozoans, 4 myxozoans, 5 digeneans, 3 monogeneans, 2 cestodes, 6 nematodes, 2 acanthocephalans, 3 crustaceans and 1 hirudinean. The crustacean Caligus lacustris occurred in both habitats while 2 other crustacean species, 2 acanthocephalans and 1 hirudinean were recorded exclusively for the lake habitat. Larval as well as adult stages of the different parasite species were found, indicating that both fish species act as intermediate and final hosts in both habitats. The Kiel Canal (total of 17 parasite species) showed a lower parasite species richness for A. brama and R. rutilus (14 and 10 parasite species, respectively) than the lake (25 parasite species). A. brama had a higher parasite richness (22 species) than R. rutilus (16 species) in the lake habitat. Most parasites collected were of freshwater origin. Consequently, the observed infection pattern of both fish species in the waterway is mainly influenced by the limited salinity tolerance of freshwater parasites, which are negatively affected even by a salinity of 2.3 to 4.5. In the central Kiel Canal, neither fish species was infected with marine parasites of low host specifity. These parasites are either limited by the low salinity at this sampling site (<4.5 to 6.0) or they cannot enter the canal due to the environmental conditions prevailing in this artificial brackish water habitat. Thus, the canal may comprise a natural barrier preventing the distribution of North Sea parasites into the Baltic Sea. However, the brackish water Baltic Sea nematodes Paracuaria adunca and Cosmocephalus obvelatus were found in R. rutilus from the canal, demonstrating the ability of some parasite species to invade and extend their range of distribution through this man-made shipping route from the Baltic to the North Sea.     

Geographical patterns of parasite infracommunities in the rough scad, Trachurus lathami Nichols, in the Southwestern Atlantic ocean

We assessed temporal variability in parasite infections of rough scad (Trachurus lathami) in 3 samples from Miramar (MI) in 2008, separated by periods of 1 mo, and 2 samples from Villa Gesell (VG), 1 each in 2008 and 2009 (Buenos Aires Province, Argentina), respectively. A sample was also obtained from Cabo Frio (CF) (Brazil) in 2009 to compare differences in parasite communities between fish from this locality and each Argentinean locality. All rough scad were parasitized by at least 1 of 27 parasite species. Similarity-based multivariate analysis revealed significant differences between localities, but temporal homogeneity in each Argentinean locality. Overall, prevalence and abundance of parasite species were most similar between samples from MI and VG, while the greatest differences occurred between samples from MI and CF. A canonical analysis of principal coordinates showed significant differences among samples. Grillotia carvajalregorum was the most important species in determining the position of Argentinean samples, especially those from MI, while Ectenurus virgulus , Raphidascaris sp., and Hysterothylacium sp. were the most important species related to fish from CF. The parasite assemblage of T. lathami showed a notable temporal persistence within the same locality and a high variability at the spatial scale, suggesting the existence of 3 independent stocks of T. lathami in South Atlantic waters.     

The history of the formation of fish parasite fauna in lake Baikal

The fauna of fish parasites in Lake Baikal is represented by 5 faunistic complexes, namely the boreal plain, boreal submountain, arctic freshwater, Baikal, and Sino-Indian ones. The parasites of the boreal plain complex are dominant by the number of species (43 %). Hypotheses on the origin of the recent fish and parasite faunas of Lake Baikal were advanced on the base of the data on the parasite species composition and their distribution among hosts, as well as on the base of paleontological data. It is shown that invasion of new fish species and their parasites to Baikal led to the change of the composition of natural faunistic fish complexes and parasite systems. Invading fishes play the roles of intermediate and definitive hosts in parasite systems of Baikal, that led to the change of the initial structure of these systems.