Linking copepod functional traits to diel vertical migration at the Patagonian shelf-break

doi:10.21203/rs.3.rs-4906994/v1

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Linking copepod functional traits to diel vertical migration at the Patagonian shelf-break

https://doi.org/10.21203/rs.3.rs-4906994/v1

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Copepod diel vertical migration (DVM) is a significant phenomenon in marine ecosystems that could have implications for the biological pump and pelagic food webs. DVM has been reported in many regions of the global ocean; nevertheless, their drivers and ecological meaning are not fully understood. This study focused on the daytime and nighttime vertical abundance of select species (and developmental stages) to investigate the role of functional traits such as spawning strategy, body size, trophic group, and feeding mode in DVM at the Patagonian shelf-break (44ºS–47ºS and 60ºW–61ºW). Only females and late copepodites exhibited a normal DVM, being more abundant near the surface during the nighttime and below the thermocline during the daytime. Those species that are sac-spawners, detritivores, carnivores, omnivores, herbivores-omnivores, and cruise-feeders, such as Clausocalanus brevipes, C. laticeps, Aetideus armatus, and Oithona atlantica, were more abundant near the surface during the nighttime and below the thermocline during the daytime. Conversely, those species that are broadcasters, large-sized, herbivores, and filter-feeders, such as Calanus simillimus, Rhincalanus gigas, and Subeucalanus longiceps, did not show consistent DVM patterns, and were more abundant above the thermocline and at the fluorescence maxima, during both daytime and nighttime. Copepod depth selection appears to be influenced by a combination of morphological, physiological, behavioral, and life history traits.

Zooplankton

sex

developmental stages

daily cycle

life strategies

Southwestern Atlantic

One of the earliest books (now considered a classic) fully devoted to plankton was “Nature Adrift” by James Fraser (1962). The title expresses the common-sense view of plankton as a myriad of tiny creatures defenseless against water movements; the name plankton emphasizes that these organisms drift where currents take them. However, although not a mistake, this view is an incomplete perception. Despite being small and weak swimmers, planktonic organisms may not simply be at the mercy of horizontal ocean flows but can actively regulate their depth in the comparatively calm vertical motion zones (e.g. McManus and Woodson 2012). The vertical velocities in the ocean are generally 1 or 2 orders of magnitude lower than the horizontal velocities (Genin et al. 2005; Stewart 2008). Accordingly, many zooplankton species can perform vertical movements, and consequently, depth is the only behaviorally controlled component of their migration (Bandara et al. 2021).

The primary drivers of these migrations are spatial and temporal variations in resources and risks. This behavior likely enhances the fitness of individuals by ensuring that benefits outweigh costs. Zooplankton exhibit a widespread tendency to make daily up and down movements, a performance known as diel vertical migration (DVM), covering several hundreds of meters each day (e.g. Naylor 2010). Most frequently, zooplankton occupy deeper waters during the daytime and near-surface waters during the nighttime, although the inverse behavior also occurs (Bandara et al. 2021).

DVM was first described in freshwater environments in the early 19th century (e.g. Cushing 1951), and by the end of that century, observations confirmed its occurrence in marine zooplankton (Naylor 2010). Several explanations, which are not mutually exclusive, to explain this phenomenon and hypotheses suggesting that environmental cues or internal circadian rhythms are triggers for DVM have been proposed (Bandara et al. 2021). Additionally, those authors suggest that DVM could be a behavior originating from genetic information expressed through an ambient driver, mainly by irradiance but also by others. Despite its complexity and variability, the bulk of evidence from experimental and field studies, as well as modeling, suggests that DVM in zooplankton is a strategy that optimizes feeding in near-surface waters when predation risk is minimized (Bandara et al. 2021).

By feeding near the surface, zooplankton produce dense fecal pellets that sink faster than dead phytoplankton do, increasing the transport of organic matter to the seafloor. DVM adds an active component to this process because, by the time that food has been digested and fecal pellets are formed, zooplankton have descended hundreds of meters, transporting the organic matter generated at the upper and illuminated ocean layers downward (Ducklow et al. 2001; Hays 2003). The organic matter transported by zooplankton serves as nourishment for benthic and deep-dwelling animals. Thus, DVM plays a crucial role in ecosystem dynamics, accelerating the downward carbon flux and promoting sequestration in sediments, a phenomenon often referred to as the "biological pump”.

Copepods, which constitute the largest proportion of zooplankton (approximately 70–90%, Turner 2004), play an important role in energy transfer within marine food webs (Hansen 2006). Their life cycle consists of multiple stages, each with distinct competencies and nutritional needs. Copepods feed on phytoplankton, detritus, or the smallest zooplankton, providing sustenance for organisms at higher trophic levels and releasing nutrients that phytoplankton can recycle (Harris et al. 2000; Valdés et al. 2018). Variations in copepod functional traits such as reproductive strategies, feeding behavior, trophic roles, and body size (Pomerleau et al. 2015; Brun et al. 2016) influence ecosystem processes such as productivity, energy transfer, and DVM dynamics (Hébert et al. 2016; Pinti et al. 2019).

South of approximately 38ºS, the Patagonian shelf-break (PSB) off southeastern South America marks the boundary between the Subantarctic shelf water (SASW) and the Malvinas Current (MC), creating a permanent thermohaline front (PSBF) and exhibiting high chlorophyll-a concentrations during springtime (Romero et al. 2006; Piola et al. 2018). This region supports significant fisheries and exhibits distinct copepod diversity and biogeographic patterns (e.g. Acha et al. 2020; Cepeda et al. in press). Copepod communities across the PSB present relatively high abundances on the outer shelf and PSBF but relatively high diversity on the oceanic side of the front (Severo et al. 2024). The seasonal distribution, abundance, and life-history traits show minimal variability all along the front, suggesting consistent community composition throughout the year (Cepeda et al. in press). However, knowledge gaps remain regarding copepod population dynamics and DVM behaviors in shelf-break regions (Cepeda et al. in press).

In general, the early paradigm in which all marine zooplankton undertake vertical migration rhythms of daily periodicity seems to require revision. Not all species, nor all life stages within a species, necessarily ascend during the nighttime; some may even descend (Naylor 2010). Our objectives were to verify the existence of copepod DVM at the PSB, and to understand the role of functional traits in this behavior considering different species and developmental stages as study cases. To accomplish this goal, we studied the daytime and nighttime vertical distribution of the adult functional traits to elucidate the DVM patterns and to enhance understanding of ecosystem dynamics within the PSB.

Data were collected aboard the R/V "ARA Austral" between October 25 and November 8, 2017, during the austral spring. The cruise focused on the area known as the "Agujero Azul" (AA), located between approximately 44ºS–47ºS and 60ºW–61ºW, and its surroundings (Fig. 1). The AA is one of the geographic priority areas defined by the Pampa Azul Initiative of the Secretary of Innovation, Science and Technology (Argentina), aiming to understand the mechanisms controlling environmental conditions in the PSB and their impact on secondary production, fisheries, and biodiversity (https://www.pampazul.gob.ar/).

Sampling was carried out along two transects (northern and southern) from the outer shelf to the MC waters, crossing the PSB, totaling 15 stations visited during both daytime and nighttime (Fig. 1). Stations sampled close to dawn or dusk were excluded from the analysis, resulting in 10 stations during the daytime (10.20–19.30 h, local time) and 10 stations during the nighttime (23.30–06.30 h, local time). Physical and chemical measurements were taken at each station employing a SeaBird CTD-rosette system equipped with a fluorometer and 12 (10 L) Niskin bottles. In our analysis, we used fluorescence data as a proxy for chlorophyll-a abundance.

Mesozooplankton sampling was performed at 4 or 5 depth strata at each station on the basis of the physical and/or fluorescence profiles, using a MultiNet® Plankton Sampler Type Midi (HydroBios) with a 0.25 m² mouth opening and equipped with 5 nets of 300 µm mesh aperture and digital flowmeters. The trawling speed was maintained at 2–3 knots, with the maximum sampling depth set at 200 m or 8–10 m above the bottom at the shallower stations. The samples were preserved on board in 4% buffered formalin in seawater.

In the laboratory, the samples were examined via a Leika S8 APO stereoscopic microscope. Subsampling was necessary for the identification and counting of copepods due to their high abundance. Each sample was homogenized in a glass beaker to ensure a random distribution of organisms. Aliquots of known volume were taken (Postel et al. 2000) until at least 100 adult copepods were included; in less abundant samples, all individuals were identified and counted. Copepod abundance was expressed as individuals per m³ (ind. m^− 3) on the basis of the water volume filtered by the net, which ranged between 82 and 294 m³. Adult copepods were identified at the species level, while copepodites were classified at the family level and grouped into early (1–3) and late (4–5) stages, following Bradford-Grieve et al. (1999) and Conway (2012).

To assess potential variations in abundance between daytime and nighttime of adults and developmental stages, permutational multivariate analysis of variance (PERMANOVA) was conducted on the basis of the fourth root-transformed abundance. Pairwise comparisons relied on 4999 permutations of residuals under a reduced model to obtain P-values. This permutation method provides the best statistical power and the most accurate Type I error (Anderson et al. 2008) and was performed using a PRIMER v6 multivariate statistics package (Clarke and Gorley 2006). Their horizontal and vertical abundance graphs were generated using the Surfer 14 software.

Since no evidence of DVM was detected in males, our analyses focused on females. The female abundance was classified using four common functional traits for copepod analysis (Kiørboe 2011; Benedetti et al. 2016): (i) spawning strategy (broadcaster, sac-spawner); (ii) body size (small: 0.72–3.09 mm, large: 3.09–7.88 mm, based on the boxplot of the respective mean and deviation (Fig. S1, Supplementary material)); (iii) trophic group (carnivore, herbivore, detritivore, omnivore, herbivore-omnivore); and (iv) feeding mode (filter-feeding, ambush-feeding, cruise-feeding). The functional traits and references for all the species are presented in the Supplementary material (Table S1, Supplementary material).

Females were employed to study the relationships among the vertical distributions of their functional traits and environmental variables. Because traits may be present in different combinations in each family, late copepodites were not included in the analysis. A principal component analysis (PCA) was performed on female traits during both daytime and nighttime, using the FactoMineR package (Lê et al. 2008) from the R program (R Development Core Team 2015). The environmental variables (temperature, density, salinity, fluorescence, and depth) were treated as quantitative supplementary variables; i.e. they do not contribute to the determination of the PCA axis but are employed in the interpretation of the results. To examine the validity of the PCA, Kaiser-Meyer-Olkin (KMO) and Bartlett’s sphericity tests were performed on the parameter correlation matrix. The KMO is an index used to establish the appropriateness of factor analysis. A high value (between 0.50 and 1.00) indicates that the factor analysis is appropriate. For Bartlett’s test of sphericity, there are two levels of interpretation: (i) H₀: there is no correlation significantly different from zero between variables, and (ii) H_a: at least one of the correlations between the variables is significantly different from zero. When the computed P is lower than the significance level = 0.05, one should reject H₀ and accept H_a, concluding that there are significant relationships between the studied variables.

To assess the role of functional traits in DVM, we focused on the abundance distribution of those indicator species identified by Severo et al. (2024) for the same cruise (Clausocalanus brevipes, Clausocalanus laticeps, Aetideus armatus, Oithona atlantica, Drepanopus forcipatus, Ctenocalanus vanus, Scolecithricella minor, Calanus simillimus, Rhincalanus gigas, and Subeucalanus longiceps). Late copepodite families (Clausocalanidae, Calanidae, and Rhincalanidae), which are also indicator taxa (Severo et al. 2024), were employed to compare their DVM patterns with those of indicator species of the same families. All these taxa emerged as the most abundant within each assemblage and, in general, in the study area (see Table 2 in Severo et al. 2024). To analyze differences in depth levels between daytime and nighttime, PERMANOVA test were conducted on the basis of the log(x + 1)-transformed abundance, and their horizontal and vertical abundance graphs were generated using the Surfer 14 software.

Figure 1 Sampling stations during the daytime (black numbers) and nighttime (white numbers) across the Patagonian shelf-break during austral spring (October–November 2017). The 200 m isobath divides approximately the outer shelf and the oceanic regimes. AA: Agujero Azul region

3.1 Diel vertical abundance distribution of females, males, and copepodites

Only female and late copepodite abundances significantly differed between daytime and nighttime (PERMANOVA, Table 1), both being more abundant near the surface during the nighttime (Fig. 2a, b).

During the daytime, female abundance was distributed at 150 m and ranged between 0.30 and 147.30 ind. m^− 3 (Fig. 2a). During the nighttime, the abundance reached a peak of 326.00 ind. m^− 3 in the upper 100 m, whereas the maximum abundance in the deep layer reached only 25.30 ind. m^− 3 (Fig. 2a). The late copepodite vertical abundance was evenly distributed during the daytime, ranging from 0.10 to 524.00 ind. m^− 3, whereas it was concentrated in the upper 50 m during the nighttime, with a peak of 326.00 ind. m^− 3 (Fig. 2b).

Males were generally less abundant than females were, with similar vertical abundance distribution between daytime and nighttime, peaking at 126.00 ind. m^− 3 during the daytime, and 96.00 ind. m^− 3 during the nighttime (Fig. 2c). Early copepodite abundance was greater in the upper 100 m during both daytime and nighttime, reaching a peak of 288.00 ind. m^− 3 (Fig. 2d).

The temperature patterns were similar during both daytime and nighttime, indicating vertically stratified condition, typically austral springtime. In the outer shelf regime, temperatures varied between 7.60ºC and 9.80ºC, with a thermocline of approximately 2.00ºC at 50 m. In the oceanic regime, temperatures ranged from 4.60ºC to 6.40ºC, with a milder thermocline due to the presence of the MC (Fig. 2).

Table 1

Results of the PERMANOVA pairwise tests used to assess differences in stage abundance between daytime and nighttime. Values in bold represent P-values lower than the significance level (0.05). t: statistic
Source of variation	t	P
Female abundance	1.74	0.01
Male abundance	1.25	0.15
Early copepodite abundance	1.16	0.26
Late copepodite abundance	1.59	0.02

3.2 Relationships between functional traits and environmental variables during the daytime and nighttime

The results of the KMO and Bartlett’s sphericity tests for each PCA are presented in Table 2, indicating the suitability of the PCA for this dataset (KMO > 0.50), and that the relationships between the studied variables were statistically significant (P < 0.05; Bartlett’s test).

The PCA biplot between functional traits and environmental variables during the daytime explained 64.61% of the total variability in the first two axes (Fig. 3a). PC1 (35.17%) was positively correlated solely with the ambush-feeding mode. PC2 (29.44%) was positively correlated with the broadcaster strategy; large-size; herbivore trophic group; filter-feeding mode; temperature and fluorescence; however, it was negatively correlated with the sac-spawner strategy; detritivore, carnivore, omnivore, and herbivore-omnivore trophic groups; cruise-feeding mode; depth, salinity, and density (Fig. 3a).

The PCA biplot between the functional traits and the environmental variables during the nighttime explained 64.35% of the total variability in the first two axes (Fig. 3b). PC1 (40.53%) was positively correlated with broadcaster and sac-spawner strategies; large-size; herbivore, herbivore-omnivore, detritivore, carnivore, and omnivore trophic groups; filter- and cruise-feeding modes; temperature and fluorescence, whereas it was negatively correlated with depth, salinity and density. PC2 (23.82%) was positively correlated solely with the ambush-feeding mode (Fig. 3b).

Table 2

Results of Bartlett's sphericity test and the Kaiser-Meyer-Olkin (KMO) sampling adequacy test for each principal component analysis (PCA). Values in bold represent P-values lower than the significance level (0.05). χ²: chi-square; Df: degrees of freedom
	Day	Night
Bartlett’s test
χ²	4110.03	3808.21
Df	136	136
P	< 0.001	< 0.001
KMO	0.52	0.53

3.3 Diel vertical abundance distribution of female indicator species and late copepodites

The vertical abundance distribution of female indicator species and late copepodites during both daytime and nighttime are depicted in Fig. 4. Clausocalanus brevipes, Clausocalanus laticeps, Aetideus armatus, Oithona atlantica, and late Clausocalanidae copepodites only exhibited significant differences between daytime and nighttime in the deeper strata (PERMANOVA, Table 3).

The broadcaster, small-size, herbivore-omnivore, and cruise-feeder C. brevipes was more abundant at 150 m during the daytime, ranging between 57.50 and 102.00 ind. m^− 3, whereas during the nighttime, it was distributed in the upper 50 m, reaching 102.00 and 124.00 ind. m^− 3 (Fig. 4a). The broadcaster, small-size, herbivore-omnivore, and cruise-feeder C. laticeps was more abundant at 150 m during the daytime, with a peak of 12.00 ind. m^− 3, whereas it reached 25.00 ind. m^− 3 in the upper 50 m during the nighttime (Fig. 4b). The broadcaster, small-size, carnivore, and ambush-feeder A. armatus, exhibited a maximum of 1.73 ind. m^− 3 near 200 m during the daytime and at 50 m during the nighttime (Fig. 4c). The sac-spawner, small-size, omnivore, and ambush-feeder O. atlantica reached 25.00 ind. m^− 3 near 200 m during the daytime, whereas it was more abundant in the upper 100 m during the nighttime (Fig. 4d). Late Clausocalanidae copepodites exhibited a maximum of 500.00 ind. m^− 3 during the daytime between 150 and 200 m, and their abundance ranged between 100.00 and 200.00 ind. m^− 3 in the upper 50 m during the nighttime (Fig. 4e).

The sac-spawner, small-size, herbivore, and filter-feeder Drepanopus forcipatus, exhibited higher abundances during the nighttime, peaking at 75.00 ind. m^− 3 in the upper 50 m (Fig. 4f). The broadcaster, small-size, herbivore-omnivore, and filter-feeder Ctenocalanus vanus reached a maximum of 130.00 ind. m^− 3 during both daytime and nighttime in the upper 50 m (Fig. 4g). The broadcaster, small-size, detritivore, and cruise-feeder Scolecithricella minor was more abundant during the daytime, with a peak of 24.00 ind. m^− 3 at 200 m (Fig. 4h). The broadcaster, large-size, herbivore-omnivore, and filter-feeder Calanus simillimus was more abundant in the upper 50 m during both daytime and nighttime, peaking at 68.00 ind. m^− 3 at 100 m during the daytime and at 50 m during the nighttime (Fig. 4i). The broadcasters, large-size, herbivores, and filter-feeders Rhincalanus gigas and Subeucalanus longiceps, were evenly distributed in the upper 50 m during both daytime and nighttime (Fig. 4j, k). Late Calanidae copepodites were uniformly distributed in the water column during the daytime, but peaked at 430.00 ind. m^− 3 in the upper 50 m during the nighttime (Fig. 4l). Late Rhincalanidae copepodites exhibited a maximum of 33.00 ind. m^− 3 between 100 and 150 m during the daytime, and in the upper 50 m during the nighttime (Fig. 4m).

The fluorescence values were greater (7.50–16.00) in the upper 50 m of the water column during both daytime and nighttime (Fig. 4). Along the northern transect, relatively high fluorescence values were generally observed on both the outer shelf and the oceanic regime, whereas along the southern transect, the maximum fluorescence occurred in the outer shelf regime.

Table 3 Results of the PERMANOVA pairwise tests used to assess differences in indicator species and copepodite abundance between daytime and nighttime. Only results with P-values lower than the significance level (0.05) are shown. t: statistic. Strata 1–2 correspond to 55–200 m of depth

Source of variation	Strata	t	P
C. brevipes	1	2.22	0.02
	2	2.19	0.03
C. laticeps	1	1.94	0.02
A. armatus	1	2.23	0.04
O. atlantica	1	2.20	0.01
	2	1.94	0.03
Late Clausocalanidae copepodites	1	2.10	0.04
	2	1.98	0.03

Studies conducted in shelf and oceanic waters worldwide have revealed the heterogeneous distribution of zooplankton across different depths (Vinogradov 1970), with DVM representing a behavior capable of modifying the vertical distribution of species. Hardy’s (1956) old statement: “There are many unsolved puzzles of pelagic natural history, but one seems perhaps more baffling than any other: that of vertical migration” remains present. Given the challenges associated with tracking individual zooplankton over space and time, much of the existing evidence for their DVM has been inferred from their vertical distribution (Bandara et al. 2021).

Our observations of copepod diel vertical distributions suggest that some species perform DVM, and that such behavior would be influenced by their reproductive, feeding, growth, and survival strategies, that is, by their functional traits.

4.1 DVM in females and late copepodites

Several authors highlighted that zooplankton do not migrate as a cohesive population (Pearre 1979; Roe 1984; Haney 1988). With respect to copepods, distinctions between males and females, as well as among different developmental stages, have been documented (Roe 1984; Uye et al. 1990; Atkinson et al. 1992; Huang et al. 1992; Osgood and Frost 1994). However, whether these differences stem from reproductive or feeding strategies remains unclear.

In this study, only females and late copepodites exhibited variations in their vertical abundances, displaying normal DVM, with higher concentrations at deeper levels during the daytime and at the surface during the nighttime (Fig. 2a, b). Similar patterns were observed in Calanus spp. and other species, where evident DVM beginning in late copepodites peaked in adult females, but was restricted or absent in males (Uye et al. 1990; Osgood and Frost 1994; Falkenhaug et al. 1997). In this sense, a gradual development of migration behavior occurs, with early copepodites aggregating in the upper water column, whereas late copepodites and adult females engage in normal DVM (Huang et al. 1992). These findings align with the developmental transition in late copepodites of Clausocalanidae shown in our results, which exhibited significant daily variations, matching those of adult females of Clausocalanus brevipes and Clausocalanus laticeps. The similarity in behavior with adult females as they develop, suggests that most late copepodites could be females, explaining their tendency to exhibit DVM. If this is the case, most of the species studied here could have genetic determination of sex. Both environmental and genetic sex determination modes have been proposed for copepods (Fleminger 1985; Mauchline 1998; Svensen and Tande 1999; Gusmão and McKinnon, 2009). Male-female ratios are biased, with females typically being more abundant (Kiørboe 2006), but there is also evidence that sex change during development is a possible mechanism for determining their sex ratio (Gusmão and McKinnon, 2009). For example, the final sex in Calanus will not be determined until stage 5 (Irigoien et al. 2000; Miller et al. 2005). At these late stages, not only their morphology but also their behavior changes. Nevertheless, little is known about the ontogenetic changes in the sensory inputs of the nervous system of copepods that could result in different DVM patterns (Ringelberg 2010).

Although a lack of DVM in males has been reported for several species, to the best of our knowledge, explanations for this remain elusive. In general, the ability of males to optimize their swimming pattern increases their chances of locating female signals but also exposes them to greater predation risk (Kiørboe 2007, 2011). The higher mortality rate among males and, consequently, their lower abundance may limit fertilization rates (Kiørboe 2007). Thus, the uniform vertical distribution observed in males (Fig. 2c) could guarantee enough chances to encounter females without moving, being less exposed to predators and saving energy.

Copepod depth selection could be viewed as a response to improve individual fitness, influencing metabolism, growth, and life cycle characteristics (Lampert 1989; Reichwaldt et al. 2005). Whatever its impact, fitness is determined by the feeding, growth, survival, and reproductive rates of organisms, which in turn depend on individual biological factors and may be expressed through a combination of morphological, physiological, behavioral, and life history traits (Litchman et al. 2013).

4.2 Role of functional traits in DVM: indicator species used as study cases

Functional traits include morphological, biochemical, physiological, structural, phenological, and behavioral characteristics, defining species in terms of their ecological roles and how they interact with the environment and other species (Díaz and Cabido 2001). These traits could influence several marine ecosystem processes, including DVM (Hébert et al. 2017).

Figure 5 schematically summarizes our main findings on the relationships between copepod functional traits and depth levels during both daytime and nighttime. During the daytime, a greater abundance of broadcaster, large-sized, herbivore, and filter-feeder species occurred above the thermocline, whereas greater abundance of sac-spawner, detritivore, carnivore, omnivore, herbivore-omnivore, and cruise-feeder species were found below the thermocline (Fig. 5). Instead, during the nighttime, a greater abundance of broadcaster, sac-spawner, large-sized, herbivore, detritivore, carnivore, omnivore, herbivore-omnivore, filter-, and cruise-feeder species occurred above the thermocline (Fig. 5). Ambush-feeder and small-sized species did not exhibit a daily depth-related pattern.

Figure 5 Schematic representation of the relationships between copepod functional traits and depth levels during the daytime (left) and nighttime (right) at the Patagonian shelf-break. The background represents the temperature, with a thermocline at 50 m separating the warmer (red) and colder (yellow) water. The triangle base (vertex) indicates where greater (lower) abundance occurred. Herb-omn: herbivore-omnivore

Four of the ten indicator species (C. brevipes, C. laticeps, Aetideus armatus, and Oithona atlantica) presented different combinations of functional traits, performed normal DVM, presented significant daily differences, and were concentrated above the thermocline during the nighttime and below it during the daytime (Fig. 4a–d).

Clausocalanus spp. usually overlap in their vertical distribution range and migration amplitude (Frost and Fleminger 1968), and exhibit greater relative abundance at shallower depths during the nighttime than during the daytime (Di Carlo et al. 1984; Peralba and Mazzocchi 2004; Brugnano et al. 2010; Feng et al. 2022). Notably, given the relatively high abundances of C. brevipes and C. laticeps (Fig. 4a, b), they strongly contributed to the DVM female signal (Fig. 2a). This herbivore-omnivore genus could adapt to a wider range of nutritional resources, given its feeding behavior on the basis of the capture of particles by direct interception (Mazzocchi and Paffenhöfer 1999). In this context, the cruise-feeding mode adopted by C. brevipes and C. laticeps could be an efficient strategy, allowing the search for a larger water volume and supporting daytime migration out of the euphotic zone, where a greater presence of visual predators is expected (Kiørboe 2011; Prowe et al. 2019). Consequently, the combination of both trophic groups and feeding strategy may enable these species to occupy different depths throughout the daily cycle.

Carnivores or omnivores such as A. armatus and O. atlantica, respectively, would be less reliant on microalgal supplies than larger herbivorous calanoids, so they do not need to move to the euphotic layer every night (Fortier et al. 2001). The feeding mode is partially related to the dietary strategy; for example, filter-feeding is effective in capturing non-motile prey such as diatoms, ambush-feeders require that individuals remotely detect prey, and cruise-feeders need to collide with them (Kiørboe 2011). Moving very little and not generating feeding currents reduces copepod susceptibility to both visual and tactile predators but also decreases their rate of food intake (Paffenhöfer 1993). Although ambush-feeding did not correlate with depth in the PCA (Fig. 3), this strategy appears advantageous for the carnivore A. armatus and the omnivore O. atlantica, likely because of lower costs and risks (Saiz and Kiørboe 1995). Moreover, the act of capturing food is closely connected to the metabolic trade-off between reproduction and survival (Kiørboe and Sabatini 1994). Sac-spawner females, such as O. atlantica, are probably more susceptible to visual predators and have lower fecundity, but would be outbalanced by high brood care maternal investment (Bollens and Frost 1991).

Calanus simillimus, Rhincalanus gigas, and Subeucalanus longiceps did not exhibit detectable DVM, and occurred at depths of the fluorescence maxima (0–50 m) during both daytime and nighttime (Fig. 4i–k), which is consistent with a significant advantage for species that feed on phytoplankton (McGinty et al. 2018). Strongly significant relationships between fertility and chlorophyll-a were found for broadcasters but not for sac-spawners (Bunker and Hirst 2004). The predator-evasion hypothesis predicts that organisms would only incur the cost of residence near the surface, increasing predation risk, when it is outweighed by the benefit of near-surface foraging (Hays et al. 2001). Broadcasters have high fecundities as an adaptation to the very high mortality rates experienced by free eggs (Kiørboe and Sabatini 1995). This spawning strategy could be favorable for remaining in the upper water layer for longer times and preventing eggs being eaten with the adults, as would be the case for sac-spawners.

Our results are representative of austral springtime conditions in a temperate region, that is, at the moment of the highest chlorophyll-a abundance (Romero et al. 2006), but DVM behavior could vary during the annual cycle. For example, two of the species that we reported as non-migrant, C. simillimus and R. gigas, were observed to perform normal DVM, which is linked to feeding cycles, during the summertime in South Georgia (Atkinson et al. 1992; Ward et al. 1995). These results suggest that the behaviors we reported for the PSB may vary seasonally.

In conclusion, our findings support earlier observations on copepod DVM complexity: not all species perform DVM, and among those that do, only females and late copepodites carry out DVM. Additionally, this study revealed that copepod functional traits play important role in DVM by influencing their vertical distribution in relation to reproductive, feeding, growth, and survival strategies. Nevertheless, it is the species, not the traits themselves, that perform these migrations. In that sense, we conclude that, in general, those species combining strategies of sac-spawning and cruise-feeding, with trophic modes of detritivores, carnivores, omnivores or herbivores-omnivores, tend to be more abundant near the surface during the nighttime and below the thermocline during the daytime. On the other hand, those species that combine the strategies of broadcasting, filter-feeding and large-sized herbivores present no consistent trends in DVM.

Acknowledgements The authors would like to especially thank Pampa Azul Initiative (Secretary of Innovation, Science and Technology, Argentina) for supporting the development of this multidisciplinary cruise, and the crew and scientific staff onboard the R/V for their assistance and sample collection. This is Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP) contribution nº xx.

Funding This study was partially supported by funds from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and INIDEP. Ayelén Severo is granted by CONICET fellowship.

Conflict of interest The authors declare that they have no conflicts of interest.

Data availability The datasets generated during the current study are available from the corresponding author on reasonable request.

Ethical approval No ethical clearance was required for the zooplankton sample used in this study.

Author contributions The author and coauthors contributed to the study design, original draft writing, conceptualization, visualization, analysis, and data interpretation. Georgina Daniela Cepeda and Eduardo Marcelo Acha also significantly contributed to data acquisition, supervision, and critical revision. All the authors approved the final version of the manuscript.

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Linking copepod functional traits to diel vertical migration at the Patagonian shelf-break

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Abstract

Figures

1. INTRODUCTION

2. MATERIALS AND METHODS

3. RESULTS

3.1 Diel vertical abundance distribution of females, males, and copepodites

3.2 Relationships between functional traits and environmental variables during the daytime and nighttime

3.3 Diel vertical abundance distribution of female indicator species and late copepodites

4. DISCUSSION

4.1 DVM in females and late copepodites

4.2 Role of functional traits in DVM: indicator species used as study cases

Declarations

References

Supplementary Files

Status:

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