Centropages Typicus Research Articles

Blind dating—mate finding in planktonic copepods. I. Tracking the pheromone trail of Centropages typicus

Mate-finding behaviour in the marine copepod Centropages typicus was investigated by 3-dimensional video analysis. Females leave a chemical trail in their wake and a male intercept- ing a fresh trail initiates a characteristic tracking behaviour in which he increases his speed from ~10 to ~30 mm s -1 and races up the female trail while displaying a tight zigzag motion. Within sec- onds the male overtakes the female and attempts to catch her. Males faithfully follow even very con- voluted trails and successfully track down females after pursuing trails up to 31 s old and 17 cm long. The probability of detecting a trail is inversely related to trail age and length. Males often start track- ing female trails in the wrong direction before correcting themselves, and the frequency of direc- tional errors increases with increasing trail age. Complicated or disrupted signal trails may cause males to lose the trail. This induces a distinct signal-scanning behaviour characterised by further enhanced swimming speeds of 50 to 70 mm s -1 , and frequent shifts of direction. The male scans a restricted volume around the point where the trail was lost and often regains the trail and resumes normal tracking behaviour. This behaviour may help males follow trails that are broken by turbu- lence. A simple generic model of pheromone trails that is consistent with the tracking behaviour of males in C. typicus and other species of copepods was used to explore the characteristics of pheromone trails. Model considerations suggest that these pheromones are small molecules, e.g. amino acids, and that the investment in pheromone production, both in terms of elements and metabolic energy, represents only a small fraction of the females' ingestion and metabolic rate.

Interdecadal variability in the Gulf of Maine zooplankton community, with potential impacts on fish recruitment

Abstract We used principal component analysis (PCA) to explore interannual changes in a time-series lasting more than 40 years of zooplankton abundance from NOAA's Continuous Plankton Recorder (CPR) survey. This analysis identified a complex of taxa, including Centropages typicus, Oithona spp., Pseudocalanus spp., and Metridia lucens that followed a common pattern of interdecadal variability characterized by a dramatic increase in these taxa around 1990, followed by a rapid decline in 2002. All of these taxa showed a large proportional increase in winter abundance between the 1980s and 1990s. These changes could be driven by increased primary productivity during winter, caused by a large-scale freshening of the Northwest Atlantic Shelf. In addition to the “community shift” mode, the analysis found a strong mode of interannual variability attributed to previously described changes in the abundance of late-stage Calanus finmarchicus. To explore the impact of these modes on higher trophic levels, we correlated the zooplankton modes with recruitment time-series from 12 fish stocks from the Gulf of Maine region. Several significant correlations were found, suggesting that the changes in the zooplankton modes may reflect broad changes in the Gulf of Maine ecosystem.

Spatial distribution of the copepod Centropages typicus in Ligurian Sea (NW Mediterranean). Role of surface currents estimated by Topex-Poseidon altimetry

A particle-tracking model was used to simulate the dispersion and development of the planktonic copepod Centropages typicus during spring in Ligurian Sea. We show that mesoscale current structure, with a coastal jet and eddies, plays a key role in the transport and dispersion of C. typicus during its life cycle. Although, in the north, offshore Nice, cohorts can be advected southwestward out of Ligurian basin, more to the south others are retained in the central eddy and may give the start to the spring bloom of this species. However, input of individuals from the south through the Corsican Channel and along the west coast of Corsica may also be important in spring. This study shows that the ambit of C. typicus population is larger than the Ligurian Sea. To cite this article: J.C. Molinero, P. Nival, C. R. Biologies 327 (2004).

Population structure of the copepods Centropages typicus and Temora stylifera in different environmental conditions

Population structure of the copepods Centropages typicus and Temora stylifera in different environmental conditions

Predation by calanoid copepods on the appendicularian Oikopleura dioica

Appendicularians have some of the highest growth rates among metazoans but they are usually outnumbered by the slower growing copepods in mesozooplankton communities. We present experimental evidence that the eggs and juveniles of the appendicularian Oikopleura dioica are actively consumed by various copepod species. Clearance rates of Calanus helgolandicus, Candacia armata, Centropages typicus, Eucalanus crassus, and Temora longicornis on eggs of O. dioica were usually above 300 ml copepod‐1 d‐1. The ingestion rates of C. helgolandicus on O. dioica eggs did not reach saturation even at the highest egg concentrations (4,560 eggs L‐1). Although C. helgolandicus, C. typicus, and C. armata preyed actively on 1‐mm‐long O. dioica (approximately 0.2 mm in trunk length), predatory pressure decreased with increasing appendicularian size. We suggest that the association of dense appendicularian populations with phytoplankton blooms could be explained by their opportunistic response to beneficial conditions before copepod densities become high enough to cause a decline in appendicularian populations due to predation. Our results indicate that, in addition to the direct shunt of biomass from picoplankton to fish, appendicularians can occupy a similar role to that of microzooplankton in the ocean. They represent an intermediate step in the less efficient, picoplankton‐appendicularia‐copepod‐fish food chain.

Population structure of the copepods Centropages typicus and Temora stylifera in different environmental conditions

Abstract The population structure (NI to adults) of the copepods Centropages typicus and Temora stylifera was investigated in parallel at two sites in the eutrophic and oligotrophic waters of the Gulf of Naples (Tyrrhenian Sea) with the aim of identifying the environmental factors that modulate the occurrence of these calanoids that are abundant in the neritic waters of the Mediterranean Sea. Monthly zooplankton sampling was conducted from May 1999 to June 2000 in 5–7 discrete depth layers in the upper 200 m with a 70-μm mesh net. Temperature, salinity, and fluorescence profiles were recorded by CTD casts. The remarkable differences observed in the temporal and spatial patterns of the two populations throughout their developmental cycles seem to result more from different responses to environmental factors than from different life-history traits. C. typicus was abundant in early to mid-summer and was distributed in the whole water column; T. stylifera followed in late summer–autumn and occurred preferentially in the upper 30 m. Temperature was the main regulating factor for T. stylifera. The availability of autotrophic food appeared relatively more important for C. typicus, although unequivocal signals were not observed, suggesting that more complex trophic interactions likely affect the dynamics of the two populations.

Horizontal and vertical distribution patterns, retention rates, and population dynamics of zooplankton on Western Bank, Scotian Shelf

We assess the importance of retention rates and local production to the concentration of zooplankton on Western Bank, Scotian Shelf, during September and October 1998. We do so using (i) particle retention rates derived from an array of 25 current meters and inferences from hydrographic structure; (ii) observations on the horizontal and vertical distribution of zooplankton and ichthyoplankton; and (iii) a simple projection-matrix model of the population dynamics of two copepod species, Centropages typicus and Pseudocalanus spp. Zooplankton biomass and adult stages of copepods were more abundant in surface waters on the bank (p < 0.05) at broad (25 km) spatial scales. Zooplankton was correlated with ichthyoplankton abundance at this scale (r > 0.5, p < 0.001), a result of local production of both zooplankton and fish on the bank. The time-dependent anticyclonic circulation around Western Bank was variable, and particle retention rates were 18 and 33% for 20 days at 12.5 and 28.5 m, respectively. The population model showed that both C. typicus and Pseudocalanus spp. are capable of increasing their population size despite advective loss and mortality rates approaching 10%·day-1. We conclude that local production exceeding advective loss rates can explain the high concentrations of zooplankton on Western Bank.

Annual Cycle of Zooplankton Biomass, Abundance and Species Composition in the Neritic Area of the Balearic Sea, Western Mediterranean

Abstract. Seasonal changes in zooplankton biomass, abundance and species composition were studied at a neritic station in the Balearic Sea between April 1993 and May 1994. Sampling was carried out every 10 days in a zone influenced by the main current circulating through the Mallorca channel. Three main peaks of zooplankton biomass and abundance were observed: (1) at the beginning of summer when the thermocline developed, (2) in autumn when the thermocline broke down, and (3) in early spring. The smaller zooplankton fraction (100–250 μm) comprised on average 32 % of the total biomass and 73 % of total abundance. Copepods were the predominant group (64 % of the total abundance) with Clausocalanus, Oithona and Paracalanus being the most abundant genera. Paracalanus parvus, Clausocalanus furcatus, Acartia clausi, Oithona plumifera, Temora stylifera, Centropages typicus and Oncaea mediterranea were found to be the most important species in the area. Other abundant groups were cladocerans (15 %) and meroplankton larvae (12 %), both of which were particularly numerous during the stratified period. The copepod community was characterized by the above‐cited perennial species, which were abundant during the cycle studied. However, the influence of the hydrological conditions of the Balearic Sea, such as the Atlantic water influx and the physical structure of the water column (stratification and mixing), promoted the observed variability in zooplankton as well as the appearance of characteristic species during the annual cycle.

Effects of small‐scale turbulence on copepods: The case of Oithona davisae

We report the effects of small‐scale turbulence on the feeding rates of the marine copepod Oithona davisae. Laboratory experiments were conducted under a range of turbulence dissipation rates between 10−4 and 101 cm2 s−3. Net enhancements of feeding were observed only at the lowest, whereas negative net effects appeared only at the highest, turbulence intensities. These results contrast with expectations from an encounter‐based model for this copepod species that predicted positive feeding enhancements at all turbulence intensities. This disagreement suggests the presence of detrimental effects at moderate and high turbulence intensities, very likely driven by either a lower mechanosensor perception capability or lower capture success. In comparison to other ambush copepods, O. davisae appears much more sensitive to the presence of turbulence, which might be the result of its strict ambush behavior, whereas copepods like Acartia tonsa or Centropages typicus, which can switch into different feeding modes, appear to benefit more from turbulence. The response of O. davisae feeding to turbulence in our experiments agrees with recent field observations on changes in the vertical distribution of Oithona as a function of wind‐driven turbulence events. Hence, O. davisae seems to choose those depths where small‐scale turbulence favors feeding.

Viability of dinoflagellate cysts after the passage through the copepod gut

Several dinoflagellate species form nonmotile, thick-walled resting cysts in their life cycle. Cysts can be ingested by planktonic and benthic organisms, but there is scarce information concerning their survival after the passage through the digestive apparatus of the grazers. We tested the germination capability of cysts produced by two neritic dinoflagellates, Scrippsiella trochoidea (F. Stein) A.R. Loeblich and Scrippsiella ramonii Montresor, after their ingestion by four copepod species. Experiments have been carried out with four species: Acartia clausi Giesbrecht, 1889; Centropages typicus Kröyer, 1849; Temora stylifera Dana, 1849; and Clausocalanus lividus Frost and Fleminger, 1968. Copepods were fed either with motile cells or cysts, and feeding and clearance rates were estimated for A. clausi, C. lividus and T. stylifera. Grazing rates on both dinoflagellates was much higher for vegetative cells than for cysts. Resting cysts were isolated from the faecal pellets and incubated to test their germination capability. S. trochoidea cysts eaten by C. typicus and T. stylifera showed a high germination rate, while cysts of the same species were not viable after the passage through the gut of A. clausi and C. lividus. In contrast, S. ramonii cysts were never able to germinate after being ingested by copepods. The observed variation in viability among the two cyst types and the different survival rates observed for S. trochoidea cysts might be related to differences in cyst morphology and to differences in the digestive process among the tested copepod species.

Motility of copepod nauplii and implications for food encounter

MEPS Marine Ecology Progress Series Contact the journal Facebook Twitter RSS Mailing List Subscribe to our mailing list via Mailchimp HomeLatest VolumeAbout the JournalEditorsTheme Sections MEPS 247:123-135 (2003) - doi:10.3354/meps247123 Motility of copepod nauplii and implications for food encounter Josefin Titelman1,2,3,*, Thomas Kiørboe1 1Danish Institute for Fisheries Research, Department of Marine Ecology and Aquaculture, Kavalergården 6, 2920 Charlottenlund, Denmark 2Göteborg University, Department of Marine Ecology, Kristineberg Marine Research Station, 450 34 Fiskebäckskil, Sweden 3Present address: Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3DH, United Kingdom *Email: joti@pml.ac.uk ABSTRACT: Velocity differences drive all encounter processes. Therefore, knowledge of both prey and predator motility are essential in order to understand feeding behavior and predict food acquisition rates. Here, we describe and quantify the motility behavior of young and old naupliar stages of 6 copepods (Centropages typicus, Calanus helgolandicus, Temora longicornis, Acartia tonsa, Eurytemora affinis and Euterpina acutifrons). Behaviors of individual nauplii were divided into sequences of sinking, swimming and jumping events. Motility behavior is both stage- and species-specific in terms of appearance of tracks, speeds, durations and frequencies of events as well as time budgets. Motility mode often changes drastically during naupliar ontogeny. Crudely, nauplii can be divided into those moving with a jump-sink type of motility of various frequencies (1 min-1 to 3 s-1) and those swimming with a smoother glide of varying continuity. We apply observed time budgets and behavior-specific speeds in simple models to examine mechanisms of food encounter. The motility of all nauplii may account for clearance rates reported in the literature, but through different mechanisms. Smoothly swimming nauplii encounter food by scavenging, which also allows for some food capture inefficiency. Jump-sink types rely on motile food. We demonstrate how diffusivity of motile prey may account for observed clearance rates for jump-sink types, which seem to employ 2 strategies. Infrequent jumping as observed in many cyclopoids is sufficient to prevent prey diffusion from reaching steady state rates, which are too low to account for observed clearance rates reported in the literature. Frequent jumpers (e.g. Acartia tonsa) jump at a frequency close to the optimum required to maximize the use of prey motility and to avoid local food depletion. KEY WORDS: Nauplii · Copepod · Motility · Behavior · Food encounter · Clearance rate · Volume encounter · Predator prey interaction · 3D Full text in pdf format PreviousNextExport citation RSS - Facebook - Tweet - linkedIn Cited by Published in MEPS Vol. 247. Online publication date: February 04, 2003 Print ISSN: 0171-8630; Online ISSN: 1616-1599 Copyright © 2003 Inter-Research.

Spectral sensitivity of vertically migrating marine copepods.

Light is a critical factor in the proximate basis of diel vertical migration (DVM) in zooplankton. A photobehavioral approach was used to examine the spectral sensitivity of four coastal species of calanoid copepod, representing a diversity of DVM patterns, to test whether species that migrate (nocturnal or reverse DVM) have response spectra that differ from non-migratory surface dwellers. The following species were given light stimuli at wavelengths from 350 to 740 nm, and their photoresponses were measured: Centropages typicus (nocturnal migrator), Calanopia americana (nocturnal migrator), Anomalocera ornata (reverse migrator), and Labidocera aestiva (non-migrator). Centropages typicus and A. ornata had peak responses at 500 and 520 nm, respectively, while Calanopia americana had maximum responses at 480 and 520 nm. Thus, the species that undergo DVM have peak photobehavioral responses at wavelengths corresponding to those available during twilight in coastal water, although the range of wavelengths to which they respond is variable. Non-migratory surface-dwelling L. aestiva had numerous response peaks over a broad spectral range, which may serve to maximize photon capture for vision in their broad-spectrum shallow-water habitat.

Variations in the abundance of Centropages typicus and Calanus helgolandicus in the North Sea: deviations from close relationships with temperature

The interannual variations in abundance of the calanoid copepod Centropages typicus (Kroyer) in the North Sea are significantly positively correlated with sea-surface temperature. The same is true of Calanus helgolandicus Claus. In both cases there was a deviation from the close relationship with temperature for several years in the early to mid-1980s. Centropages typicus was less abundant than expected from 1981 to 1984, but Calanus helgolandicus recovered from a period of lower than expected abundance from 1980 to 1982, to become more abundant than expected from 1983 to 1987. The difference between the responses of the two species to climate-driven changes in seasonal cycles of phytoplankton is interpreted in relation to their biology. Geographical variations of the interannual variability and seasonal cycles of Centropages typicus in the North Sea are analysed. The centre of the population of this species in the North Sea is in the German and Southern Bights, but the variations in abundance may be partly influenced by advection from areas to the west of Britain.

Copepod egg production in the NW Mediterranean: effects of winter environmental conditions

In the NW Mediterranean the highest abundance of phytoplankton is found during late winter, when temperatures are low. During summer, on the other hand, temperatures are high and phytoplankton abundance low, resulting in low copepod egg production rates (EPR). Despite the apparently better food conditions for copepod growth during winter, we lack information on copepod EPR during the cold season and on the possible effect temperature has on inhibiting this metabolic rate. To solve this uncertainty, a study was carried out to assess the effects exerted by the winter envi- ronmental conditions on the EPR of 3 representative planktonic copepod species of the NW Mediter- ranean (Centropages typicus, Clausocalanus lividus, Acartia clausi). The data were collected during 2 oceanographic cruises in March 1999 (Hivern-99) and January-February 2000 (Hivern-00) and the results compared to those of typical summer conditions. During the Hivern-99 cruise the phytoplank- ton abundance was very high (ranging from 1 to 1.5 µg > 5 µm chlorophyll a (chl a) l -1 ), indicating bloom conditions. During the Hivern-00, the phytoplankton bloom had not yet developed, evident by the chl a concentration of ~0.5 µg l -1 . The recorded EPR during Hivern-99 were amongst the highest for the studied species, and the clearance rates deduced from them indicate a shorter (phytoplankton - copepods) food web during the winter phytoplankton bloom than for the rest of the year, when the planktonic trophic interactions take place through a longer microbial food web.

Time series analysis of interrupted long-term data set (1961-1991) of zooplankton abundance in Gulf of Maine (northern Atlantic, USA)

The main interannual and seasonal signals have been extracted from a multi-decadal data set of zooplankton collected with the Continuous Plankton Recorder in the Gulf of Maine, from January 1961 to December 1991. The monthly abundances of seven species or genera of copepods representing the dominant biomass in the area were considered. The presence of a large consecutive gap (35 months) prevented the use of statistical methods for the prediction of missing data. The eigen-vector filtering (EVF) method was then used on the original time series, while retaining the missing values. For each zooplankton taxon, two principal modes of variability ( F 1 and F 2) were extracted, representing the interannual and seasonal variations, respectively. Results of EVF allowed the classification of the different genera or species, according to their main type of variability, into taxa ‘interannually dominated’ ( C. finmarchicus, Metridia lucens, Oithona spp.), ‘seasonally dominated’ ( Centropages typicus), and taxa characterized by both ‘interannual and seasonal variation’ ( Pseudocalanus spp., Temora longicornis, Acartia spp.). A comparison between the interannual trends of ‘interannually dominated species’ and sea surface temperature (SST) indicated that all the species were more or less correlated with this important environmental factor. In particular, a strong negative correlation was found between C. finmarchicus and SST at a lag of about 0 months, showing that lower values of SST correspond to higher abundances of Calanus finmarchicus at this latitude.

Variations of zooplankton in the frontal area of the Alboran sea (Mediterranean sea) in winter 1997

Zooplankton from the upper 200 m of the Almeria-Oran frontal region, (east of the Alboran sea, western Mediterranean) was sampled during winter 1997, using two nets equipped with 200 and 80 μm mesh. Eight sites representative of the different hydrodynamic structures (Mediterranean water, geostrophic Atlantic jet, associated anticyclonic gyre) were investigated over 2 d, using two day- and two night-samples per site. Zooplankton biomass was correlated to chlorophyll abundance, with lowest values in the oligotrophic Mediterranean water and highest in Atlantic water. The high biomass resulted from the enhancement of the secondary production, as indicated by the greater proportion of nauplii and the increase of zooplankton metabolism and feeding. Total abundance and biovolume of organisms varied like their biomass. Maximum quantitative values were recorded in the material collected by the 80-μm net which sampled more efficiently young developmental stages such as nauplii. Copepods accounted for 60–71 % of the zooplankton, and their nauplii, scarce in the 200-μm net material, up to 33 % in the 80-μm samples. Compared to the average repartition of total zooplankton at the different sites, nauplii, siphonophora, chaetognatha, ostracoda and meroplankton were preferentially distributed in the Atlantic sites. The general aspect of the copepods assemblage was homogeneous, the bulk of the population being constituted of Clausocalanus and Oithona spp. Nevertheless, the specific diversity was greater in the Atlantic waters, with the addition of some scarce species absent from the Mediterranean water. Several other species, present at every site were significantly more abundant in the Atlantic waters, e.g. Pleuromamma borealis and Eucalanus crassus. The distribution of Centropages typicus and Clausocalanus furcatus was more specifically linked to the front limit where these species could find favourable feeding conditions.

Predation by omnivorous copepods on early developmental stages of Calanus finmarchicus and Pseudocalanus spp.

Predation is thought to be an important source of mortality in the early life stages of fish and copepods on Georges Bank. Omnivorous copepods may be predators on copepod eggs and nauplii, but data on feeding rates or selectivity are scarce. As part of the GLOBEC Georges Bank program, we generated functional response curves for the omnivorous copepods Metridia lucens, Centropages typicus, and Temora longicornis feeding on the eggs and nauplii of Calanus finmarchicus or Pseudocalanus spp. in shipboard predation trials. Neither C. typicus nor M. lucens reached saturation feeding on Calanus eggs until prey concentration was >400 L−1. Individual M. lucens and C. typicus ingested up to 34 ± 9 (mean ± SD, n = 3) and 24 ± 14 eggs d−1, respectively (68C). T. longicornis was more abundant in late spring, when they ingested Calanus eggs at rates similar to those of C. typicus. At ambient prey concentrations, ingestion rates of Calanus nauplii were higher than rates of Calanus eggs for the predator M. lucens but were similar for C. typicus. Advanced naupliar stages were less susceptible to predation than young stages. Pseudocalanus nauplii moved faster and were ingested at lower rates than similarly sized Calanus nauplii. Predation rates increased with increasing temperature for the warm‐water species C. typicus but decreased for the cold‐water species M. lucens. These results may contribute to models predicting the development of copepod populations and their availability to larval fish.

Seasonal Cycles of Egg Production of Two Planktonic Copepods, Centropages typicus and Temora stylifera, in the North-western Mediterranean Sea

Reproduction of the dominant copepods Centropages typicus and Temora stylifera was studied at a permanent station in the Ligurian Sea (NW Mediterranean). Seasonal patterns of egg production, clutch size, egg size and female prosome length were followed from January 1998 to December 1999. Female carbon content and weight-specific egg production were compared in autumn 1998 and spring 1999. Reproductive patterns of C. typicus and T. stylifera were very similar, indicating that reproduction was affected by the same environmental factors. Reproductive activity was highest in autumn in both species and years. A second peak of egg production was observed in early summer, which was less intense in 1999 after a bloom of salps. Egg production rates reached maximal values of 33.5 and 33.3 eggs female-1day-1 and annual means of 10.8 and 11.7 eggs female-1day-1 in Centropages and Temora, respectively. Maximal weight-specific egg production was 0.21 day-1 in both species in November 1998, when female carbon contents were 6.7 (C. typicus) and 12.0 µg C (T. stylifera). No statistical relationship between egg production and food availability or temperature was detected. Reproductive activity did not reflect the seasonal abundance patterns, with C. typicus dominating in spring and T. stylifera in autumn.

Observations of copepod feeding and vertical distribution under natural turbulent conditions in the North Sea

We present results of simultaneous measurements of turbulent-dissipation rate, zooplankton vertical distribution and copepod gut pigments in the northern North Sea. Analysis shows that some, but not all, copepods (by species, sex and stage) exhibit significant dependence on turbulence in respect to vertical distribution and feeding rate. Oithona similis (female and copepodite stages) exhibits an avoidance of the surface layer when turbulence is strong there. For the range of turbulence (10−7 to 10−3 m2 s−3) and ambient chlorophyll concentration (0.5–0.8 μg l−1) encountered, Calanus spp. and Metridia lucens exhibited a significant negative response in feeding-rate index with increasing turbulence. Centropages typicus and Pseudocalanus spp. also exhibited a negative response but of less significance.

Zooplankton Community During the Transition from Spring Bloom to Oligotrophy in the Open NW Mediterranean and Effects of Wind Events. 1. Abundance and Specific Composition

Short-term changes in the zooplankton community were investigated at a time-series station in the open NW Mediterranean during the DYNAPROC cruise programme (May 1995). Based on the samples obtained with three devices (12 l bottle, 200 μm and 500 μm mesh nets), the abundance and specific composition are preseuled for mesozooplankton (copepods mainly), macroplankton and micronekton. Over the 3 week sampling period, overall density of the copepod community decreased and changes in the specific composition occurred. The decline was also observed in nauplii and was more marked in small-sized copepod species than in larger ones; one species, Centropages typicus, even disappeared. An increase in the proportion of carnivorous organisms appeared in both copepods (Euchaeta acuta, Heterorhabdus spp.) and euphausiids (Nematoscelis megalops, Stylocheiron longicorne). These changes are discussed in relation to environmental features and in the context of seasonal variability, the observational period coinciding with the transition from spring bloom to oligotrophy in this area. Effects of a major wind event that appeared to have induced long-lasting changes are also explored.