# Oceanographic features boost latitudinal patterns in copepod body size distribution in the South Atlantic

Érica Becker, Luis Macedo-Soares, Catarina Marcolin, Manoela Brandão, Lars

Stemmann, Maria Mazzocchi, Andrea Freire

► To cite this version:

Érica Becker, Luis Macedo-Soares, Catarina Marcolin, Manoela Brandão, Lars Stemmann, et al. Oceanographic features boost latitudinal patterns in copepod body size distribution in the South Atlantic. Limnology and Oceanography, 2024, 69 (11), pp.2668-2679. 10.1002/lno.12694. hal-04886306

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Distributed under a Creative Commons Attribution 4.0 International License
LIMNOLOGY
and
OCEANOGRAPHY

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Linnol. Oceanogr. 69, 2024, 2668-2679
© 2024 The Author(s). *Limmology and Oceanography* published by Wiley Periodicals LLC
on behalf of Association for the Sciences of Limnology and Oceanography.
doi: 10.1002/lno.12694

# Oceanographic features boost latitudinal patterns in copepod body size distribution in the South Atlantic

Érica C. Becker ID,<fnref n="1" />,<fnref n="2" />*
Luis C. P. Macedo-Soares ID,<fnref n="1" />
Catarina R. Marcolin ID,<fnref n="3" />
Manoela C. Brandão ID,<fnref n="4" />
Lars Stemmann ID,<fnref n="4" />,<fnref n="5" />
Maria G. Mazzocchi ID,<fnref n="6" />
Andrea S. Freire ID<fnref n="1" />

## Abstract

The South Atlantic Ocean (SAO) is an under-sampled ocean where the influence of environmental drivers on copepod body size is poorly understood. This study investigated the body size distribution of copepods from 13°S to 64°S to test Bergmann's rule, which predicts the occurrence of smaller organisms in warmer areas. We hypothesized that additional influence of oceanographic features strengthens this pattern. Zooplankton were sampled during the austral summer from the chlorophyll maximum depth up to the surface, at approximately 100 m depth, using a 200-µm net. The samples were analyzed using the ZooScan imaging system and were classified using the Ecotaxa tool. We estimated copepod family abundance, biomass, and size structure, and their relationships with environmental variables were assessed through generalized linear mixed models (GLMM). Although most copepods increased in size at higher latitudes, not all families followed Bergmann's rule. Small adults of Clausocalanidae, Paracalanidae, Corycaeidae, and Oncaeidae contributed mostly in the Brazil Current (BC), while Calanidae copepodites disproportionately contributed to overall biomass, and Oithonidae adults were the most abundant in high latitudes. Copepod abundance or biomass hotspots were present in the southern limit of the warm BC, at the Subtropical Confluence Zone, and in the subantarctic waters at the Drake passage. Our results suggest that oceanographic features strengthen latitudinal body size relationships due to food availability, and the importance of different life history strategies.

Additional Supporting Information may be found in the online version of this article.

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

**Author Contribution Statement:** ÉCB: Conceptualization; Data curation; Formal analysis; Funding acquisition; Investigation; Methodology; Writing – original draft; Writing – review and editing. LCPM-S: Data curation; Formal analysis; Investigation; Methodology; Writing – review and editing. CRM: Data curation; Formal analysis; Methodology; Validation; Writing – review and editing. MCB: Conceptualization; Investigation; Methodology; Validation; Writing – review and editing. LS: Data curation; Formal analysis; Methodology; Validation; Writing – review and editing. MGM: Conceptualization; Methodology; Supervision; Validation; Writing – review and editing. ASF: Conceptualization; Data curation; Funding acquisition; Methodology; Project administration; Supervision; Validation; Writing – review and editing.

Decades-old ecological rules postulate latitudinal gradients in body size, with populations and species in the tropics generally being smaller than those at higher latitudes (Bergmann 1847). While originally limited to homeotherms, Bergmann's rule results from selection favoring larger sizes in colder environments, where organisms minimize heat loss through body surface by reduced surface/volume ratio with consequent energetic advantage (Salewski and Watt 2017). However, this rule also applies widely to ectotherms, as decreasing temperature has been shown to be the main driver of increasing body size in 83.5% of ectothermic marine crustaceans along both latitudinal and depth gradients (Atkinson 1994; Timofeev 2001). The relationship between body size and temperature has regained interest in light of global climate warming (Sommer et al. 2017). In fact, it has been suggested that this warming may select for smaller sizes (Daufresne et al. 2009; Beaugrand et al. 2010; Campbell et al. 2021), with possible changes in marine community size structure that can affect regional

<footnote n="1">¹Universidade Federal de Santa Catarina, Campus Universitário, Florianópolis, Brazil</footnote>

<footnote n="2">²Istituto Nazionale di Oceanografia e di Geofisica Sperimentale, Trieste, Italy</footnote>

<footnote n="3">³Universidade Federal do Sul da Bahia, Centro de Formação em Ciências Ambientais, Rodovia Porto Seguro—Eunápolis, Porto Seguro, Bahia, Brazil</footnote>

<footnote n="4">⁴Sorbonne Université, Laboratoire d'Océanographie de Villefranche, Villefranche-sur-Mer, France</footnote>

<footnote n="5">⁵Institut Universitaire de France, Paris, France</footnote>

<footnote n="6">⁶Stazione Zoologica Anton Dohrn, Naples, Italy</footnote>

<footnote>*Correspondence: ebecker@ogs.it</footnote>
fisheries productivity and vertical carbon transport efficiency (Beaugrand and Kirby 2010; Bi et al. 2011).

Zooplankton communities exhibit larger body size and higher abundance toward the poles and tropical upwelling regions, largely driven by copepods (San Martin et al. 2006; Evans et al. 2020; Brandão et al. 2021; Campbell et al. 2021). However, recent studies have shown that biological traits and life history strategies can modify the spatial and temporal responses of marine copepods to environmental gradients (Romagnan et al. 2016). For instance, seasonal changes can lead to density-dependent effects on copepod body size reduction, ranging from ca. 3% to 10% of carbon mass per °C (Corona et al. 2021). This temperature-size response exhibits a negative correlation with total zooplankton abundance during spring in the western English Channel and is attributed to competition for food and/or intraguild predation, coinciding with the lowest ratio of food biomass to zooplankton biomass (Corona et al. 2021). In addition, a fourfold greater reduction in adult body mass per °C has been recorded in current-feeding calanoids compared to ambush-feeding cyclopoids (Horne et al. 2016). Therefore, the responses of body size to temperature gradients vary between and within taxonomic groups and are associated with different ecophysiological features that allow the organisms to cope with their environment (Ackerly and Cornwell 2007). This variation ultimately determines how they will respond to climate change.

Since the classic explanation of Bergmann's rule based on thermoregulation principles is not applicable to most ectotherms, several hypotheses have been proposed to search for alternative explanations (Vinarski 2014). According to the resource availability hypothesis, body size covaries with the length of the season, leading to smaller-sized species being prevalent both at lower latitudes, due to resource competition, and at higher latitudes, due to resource shortage after the short reproductive period during summer (Blackburn et al. 1999). The oxygen limitation hypothesis suggests that metabolism is higher at lower and warmer latitudes, which increases the individual cost of growth to a large body size (Atkinson et al. 2006). It appears that a single universal explanation for all cases of Bergmann's variation in ectotherms cannot be formulated and the distribution patterns observed most likely arise from synergic interactions between several factors that covary with latitude (Vinarski 2014).

The Western Boundary Current (WBC) of the South Atlantic Ocean (SAO) provides valuable context for understanding the influence of environmental variables on plankton size. These systems exhibit quasi-persistent fronts that delineate highly productive regions and biodiversity hotspots (Acha et al. 2004). In the SAO, examples such as the meandering of the Brazil Current and its associated seasonal intrusions of oceanic and nutrient-rich waters mirror the hydrodynamic roles played by the Gulf Stream in the southeastern USA and the North Atlantic Current, or the Kuroshio in the Pacific Ocean (Mangolte et al. 2022). The SAO is characterized by the dominance of small copepods, particularly in relatively warmer conditions where primary

production is typically low and dominated by pico- and nano-size primary producers. This pattern has been observed in several areas, including the Brazil Current (BC) (Brandini et al. 2018), the Rio de la Plata plume influence (Cepeda et al. 2020), and subantarctic frontal areas in the South Atlantic Ocean (Lopes et al. 2016). Despite the ecological importance of WBCs and their potential influence on planktonic communities, investigations into the specific characteristics of plankton size structure are lacking, particularly in comparison to the extensively studied North Atlantic counterparts.

In this study, we aimed to unravel the correlations between copepod families of different size ranges and environmental gradients from the Southwestern Atlantic Ocean to the Southern Ocean (13°S-64°S). We tested the hypothesis that copepod body size will follow Bergmann's rule at the family level, with smaller organisms contributing more in warmer locations. While our primary focus is on family-level patterns, we also aimed to determine whether different life stages, specifically adults and copepodites, contribute significantly to the observed variance in size distribution. In addition, we explore if other latitude-related factors may explain the relationship between copepod body size and environmental drivers, acting synergistically with temperature. Therefore, our study is important for broadening the scope of comparative analyses across multiple WBC features, providing a more comprehensive understanding of the general principles governing zooplankton size structure and its environmental drivers.

## Materials and methods

### Sampling strategy

A total of 37 stations were sampled during two cruises conducted in the SAO and Southern Ocean (SO) in the austral summer, from October 2010 to January 2011 (Fig. 1b,c). These stations covered a wide latitudinal range and a variety of ecosystems, from tropical (~13°S) to polar oceanic waters (~64°S). The upper water column is characterized by the southward flowing BC, while the Malvinas (Falklands) Current (MC) flows equatorward, transporting water from the Antarctic Circumpolar Current (ACC). At approximately 36°S-38°S, the MC encounters the BC, forming the Subtropical Confluence Zone (SCZ) (Fig. 1a). The MCT-II *Cruzeiro do Sul* expedition took place across the Brazilian tropical and subtropical continental shelves. The latitudinal gradient was extended during the *Tara Oceans* expedition with sampling at stations that were representative of the main basins, that is, TARA_073 to TARA_080 for SAO and TARA_082 to TARA_089 for SO.

Vertical profiles of temperature, salinity, fluorescence, and dissolved oxygen were obtained from the surface down to approximately 100 m depth using a SeaBird CTD profiler, coupled with sensors. During the MCT-II expedition, water samples were collected using 5-liter Niskin bottles to determine chlorophyll *a* (Chl *a*) at the deep chlorophyll maxima. Chl *a* determination followed the Welschmeyer (1994) protocol. During the *Tara Oceans* sampling, Chl *a* concentrations
<figure><img src="image_3.png" /><figcaption>**Fig. 1.** (a) Surface circulation of the South Atlantic and Southern Ocean (adapted from Stramma and England 1999; Garzoli and Matano 2011; Villar et al. 2015; Campos et al. 2017). (b) The map shows bathymetry along with the sampling stations from the *Tara* Oceans (yellow points) and (c) MCT-II *Cruzeiro do Sul* (red points) expeditions. The Brazil Current (BC), Subtropical Confluence Zone (SCZ), Malvinas (Falklands) Current (MC), and Antarctic Circumpolar Current (ACC) are indicated.</figcaption></figure>

were measured using high-performance liquid chromatography (Van Heukelem and Thomas 2001; Ras et al. 2008).

Zooplankton samples were collected from the epipelagic zone with a WP2 net (200-µm mesh size) towed vertically from 100 m in depth to the surface, and equipped with a flowmeter to measure the filtered water volume. The samples were fixed on-board with buffered formaldehyde for later

analyses. The sampling and sorting of copepods were consistent between both cruises. In the laboratory, the preserved zooplankton samples were fractionated between 1/2 to 1/32 using a Motoda splitter. From each fraction, an aliquot was randomly taken. The fractioning and the volume of the aliquot depended on the concentration of the original sample. Aliquots of 10 mL were used for highly concentrated
samples, while up to 30 mL was used for less concentrated samples to obtain an average of 150 copepod individuals sorted per subsample for identification (Frontier 1981). The total abundance of copepods was calculated based on the counts from each aliquot and estimated for the entire sample. This process ensured that an accurate representation of the copepod population was obtained, accounting for variations in sample concentration. On average, 4% of the total sample volume was analyzed to determine copepod abundance.

For further details on laboratory work and copepod size estimates, see Supporting Information “Copepod data.”

## Statistical analyses

Generalized linear mixed effects models (GLMMs) were applied to test if the copepods' body size in the South Atlantic Ocean followed Bergmann's rule. GLMMs extend traditional linear models by incorporating the variance of random predictor variables (Bolker et al. 2009; Zuur et al. 2009). The relationships between temperature (°C), salinity, oxygen (mg L⁻¹), and Chl *a* (mg m⁻³) and mean body size (ESD mm) were assessed among different copepod families along the latitudinal gradient in the SAO and SO (13°–64°S).

To test the relationship between environmental variables and latitude, Pearson's correlations were used. However, since correlation coefficients only show pairwise correlations, variance inflation factors (VIF) were used to determine which explanatory variables were collinear and should be removed before starting the models (Zuur et al. 2009). Our approach involved iteratively removing one variable at a time, recalculating VIF values, and continuing this process until VIF values were lower the threshold of 5. Initially, we attempted to include all environmental variables—temperature, salinity, Chl *a*, and oxygen—together in a single model. However, the model fit diagnostics were not satisfactory, likely due to significant collinearity among the variables. To address this, we decided to fit separate models for each environmental variable. This decision improved the model fit significantly, allowing us to better isolate and interpret the individual effects of each variable on copepod body size and distribution. For further details on the analytical framework, see Supporting Information “GLMMs.”

All the analyses were conducted using the statistical software R version 4.3.0 (R Core Team 2021) with the “glmmTMB” package (Magnusson et al. 2017), and model validations were checked using the “DHARMa” package (Hartig and Hartig 2017).

## Results

### Oceanographic and environmental features

The oceanographic conditions varied considerably across the region studied, which covered a vast latitudinal gradient (~52°) that extended from water influenced by the South Equatorial Current (SEC) to the Antarctic Circumpolar Current (ACC) (Fig. 1a). Temperature and salinity decreased from tropical to polar waters (Fig. 2a,b), while oxygen and Chl *a* increased

(Fig. 2c,d). The highest temperature and salinity values were found within the tropical circulation of the BC (T: ~25°C; S: ~37), observed near the tropics. Along the BC, lower Chl *a* levels (<0.5 mg m⁻³) were recorded, with a peak at 25°S (1.9 mg m⁻³). The SCZ between 35°S and 47°S was characterized by high environmental variability, with temperature ranging from 12°C to 19°C, salinity below 36, oxygen values between 7 and 8 mg L⁻¹, and higher Chl *a* concentrations (0.5–1 mg m⁻³). Moving toward the subantarctic waters of the MC, salinity was lowest (<33), temperatures ranged between 5°C and 7°C, and oxygen almost reached 10 mg L⁻¹. The SO featuring the ACC frontal system had the lowest temperature (~2°C) and salinity (~34) values. The ACC had intermediate Chl *a* concentrations, and peaks at 64°S of both Chl *a* (2 mg m⁻³) and oxygen (11.2 mg L⁻¹).

### Copepod distribution

The copepod dataset, which includes over 11,200 images obtained from ZooScan, represents three orders and 25 families (Supporting Information Fig. S1). Copepodites prevailed in the SCZ, MC, and ACC waters, whereas adult copepods prevailed in the BC area, with the exception of the zone between 27°S and 28°S (Supporting Information Fig. S2) owing to the great contribution of Clausocalanidae copepodites in this location.

The small adult copepods were the most abundant, especially in the BC area, and were dominated by Acartiidae, Clausocalanidae, Paracalanidae, Corycaeidae, Oncaeidae, and Oithonidae. These families had narrow body size ranges (Supporting Information Fig. S3) and a widespread latitudinal distribution (Supporting Information Fig. S4a). Their generally low biomass was, however, high in the SCZ region (Supporting Information Fig. S5a). Community composition shifted southwards from the SCZ (47°S), where Oithonidae became dominant. Large-sized families corresponded mainly to Calanidae, Eucalanidae, Euchaetidae, Metridinidae, Candaciidae, Scolecitrichidae, and the cyclopoid Sapphirinidae. These families had wide body size ranges (Fig. 3; Supporting Information Fig. S3), narrower latitudinal distribution (except Calanidae), and reached higher abundances between SCZ and ACC at 60°S (Fig. 4; Supporting Information Fig. S4a). These families displayed multimodal large size ranges, possibly indicating the presence of different genera or species within the family.

Clausocalanidae copepodites were abundant and had a large biomass in the BC zone, while Calanidae copepodites increased poleward, showing a substantial contribution to biomass values (Fig. 4b). Euchaetidae adults and copepodites showed low abundances but large biomass toward the equator (13°S–21°S). In contrast, Acartiidae increased at the southern limit of BC (31°S–35°S).

Some families were rare, that is, the calanoid Fosshageniidae, Lucicutiidae, Centropagidae, Heterorhabdidae, Pontellidae, Augaptilidae, Rhincalanidae, the cyclopoid Lubbockiidae, and the harpacticoid Ectinosomatidae and Tachidiidae. These families (“others” in Fig. 4) had relatively low abundance and biomass values across the entire latitudinal gradient, with the
<figure><img src="image_4.png" /><figcaption>**Fig. 2.** Latitudinal distribution of environmental variables in the South Atlantic and Southern Ocean (13°S–64°S). (a) Temperature (°C), (b) salinity, (c) oxygen (mg L⁻¹), and (d) Chl *a* (mg m⁻³) are presented from the surface down to approximately 100 m depth. The black ellipses in the temperature values indicate the oceanographic features considered in this study (see Fig. 1a), including Brazil Current (BC), Subtropical Confluence Zone (SCZ), Malvinas (Falklands) Current (MC), and Antarctic Circumpolar Current (ACC). The box plots summarize data distribution.</figcaption></figure>

exceptions of Centropagidae at 55°S and adult Rhincalanidae biomass at 60°S and 64°S.

Overall, the abundance and/or biomass of copepod families mainly peaked near the southern limit of BC waters (~25°S–30°S), southwards of the SCZ (~45°S), and in the Drake Passage (~60°S) (Supporting Information Fig. S6a,b). The community mean body size increased toward high latitudes (Supporting Information Fig. S6c), but the distribution of body size varied at the family level. Families with body size < 1 mm presented either a weak or no latitudinal gradient (Supporting Information Fig. S6d). Among the families with mean body size > 1 mm (Fig. 3), only Calanidae was distributed across the full latitudinal range, therefore driving the general increase in mean copepod body size at the high latitudes (Supporting Information Fig. S6d), which was boosted by the biomass of large adult Rhincalanidae in the ACC zone (Fig. 4a).

The GLMM results revealed a significant statistical contribution of several families to the modeled mean body size across different environmental gradients, such as temperature,

salinity, oxygen, and Chl *a*. The families Calanidae, Metridinidae, Acartiidae, and Clausocalanidae showed an increasing body size as temperature decreased along the latitudinal gradient (Fig. 5), whereas Scolecitrichidae and Sapphirinidae presented the opposite trend with steeper positive slopes (Supporting Information Table S1). Salinity distribution showed similar patterns as temperature, and the above-mentioned copepod families displayed significant increasing or decreasing latitudinal trends (Supporting Information Fig. S7).

Mean body size was generally higher in more oxygenated waters (Fig. 6; Supporting Information Table S1) and the patterns were significant for Calanidae, Metridinidae, Acartiidae, and Clausocalanidae. In contrast, Scolecitrichidae, Temoridae, and Sapphirinidae decreased significantly in body size at higher oxygen levels. The families Calanidae, Metridinidae, Acartiidae, and Paracalanidae showed a significant increasing trend with enhanced concentrations of Chl *a* (Supporting Information Fig. S8), whereas Scolecitrichidae
<figure><img src="image_5.png" /><figcaption>**Fig. 3.** Frequency distribution of copepod family body sizes, including copepodites and adults, estimated using equivalent spherical diameter (ESD), along the latitudinal gradient of the South Atlantic and Southern Ocean (13°S–64°S). The Brazil Current (BC), Subtropical Confluence Zone (SCZ), Malvinas (Falklands) Current (MC), and Antarctic Circumpolar Current (ACC) are indicated (see Fig. 1a).</figcaption></figure>

and Sapphirinidae showed a significant decreasing trend. Families exhibiting no clear trends, such as Eucalanidae, Paracalanidae, Oithonidae, and Oncaeidae, were not significant in the models.

Finally, Akaike's Information Criterion used to rank competing models highlighted that temperature was the most important predictor for optimizing model fit and complexity, followed by oxygen and salinity, whereas Chl *a* was the least important driver (Supporting Information Table S2).

## Discussion

Family-level taxonomic resolution offers new perspectives to the latitudinal pattern of copepod body size distribution in the South Atlantic. Currents and frontal systems emerge as

important factors that modulate the classical pattern of Bergmann's rule. We show that these oceanographic features amplify the general latitudinal gradient in copepod body size, particularly in areas characterized by pronounced fronts, confluence, and transitional zones. In general, our analyses reveal that temperature and salinity conform to classical expectations, smaller body sizes are observed in the tropics, and higher Chl *a* and oxygen levels are associated with families with larger average body size. However, we also observed that certain families do not show a clear latitudinal pattern, and others do not occur across the whole latitudinal gradient.

The different body size patterns among copepod families highlight the complexity within the group, emphasizing the need to consider these assemblages not as a whole but with its
<figure><img src="image_6.png" /><figcaption>**Fig. 4.** (a) Relative abundance and (b) biomass of the dominant copepod families and life stages along the latitudinal gradient in the South Atlantic and Southern Ocean (13°S–64°S). The Brazil Current (BC), Subtropical Confluence Zone (SCZ), Malvinas (Falklands) Current (MC), and Antarctic Circumpolar Current (ACC) are indicated (see Fig. 1a).</figcaption></figure>

components, at least at the family level, for a comprehensive understanding of their responses to environmental conditions and changes. We propose that the explanation for the patterns observed may lie in a combination of oceanographic, ecological, and climate drivers.

## Oceanographic drivers

Regional oceanographic features appear to boost the latitudinal patterns of copepod distribution, causing increases in biomass and/or abundance in the confluence and frontal systems of subtropical and sub-Antarctic waters, as well as in the connecting region between the Atlantic and Pacific oceans at the Drake Passage (Fig. 1a).

The latitudinal gradient in body size is a well-established biogeographic pattern, and temperature has consistently been demonstrated as a strong predictor of body size in pelagic copepods worldwide (Evans et al. 2020; Brandão et al. 2021; Campbell et al. 2021; Corona et al. 2021). Interestingly, our research reveals that the effect of the latitudinal gradient was only pronounced among some copepod families, particularly in the biomass-dominant Calanidae, mainly due to the high contribution of copepodite stages. This suggests that the general relationship between size at the community level and temperature provides only a partial explanation and cannot be universally applied to all copepod families.
<figure><img src="image_7.png" /><figcaption>**Fig. 5.** Mean body size (ESD mm) of copepod families along the temperature (°C) gradient in the South Atlantic and Southern Ocean (13°S–64°S). Solid lines represent the fitted values (± 95% CI, colored shading) predicted for each family using GLMM models. The corresponding *p* values, denoting statistical significance, are indicated at the top left corners: *p* < 0.1; \* *p* < 0.05; \*\* *p* < 0.01; \*\*\* *p* < 0.001. Please note that the y-axis scale varies among the families due to their different body size ranges.</figcaption></figure>

The latitudinal extent comprises macroscale environmental gradients and it also includes highly dynamic oceanographic features. These conditions appear to promote increases in biomass and/or abundance and impact the distribution of average body size in most copepod families along the latitudinal gradient. This outcome is influenced by the availability of nutrients and energy during the population growth seasons (Geist 1987).

Pelagic copepods rely on food sources that are brought up by water movements related to oceanographic currents and water mass interactions. Within the SAO and the SO, which collectively constitute one of the most complex and dynamic oceanographic regions of the world, numerous marine fronts cover a large range of spatial and temporal scales (Acha et al. 2004). These fronts serve as boundaries between different water masses and are likely to accommodate varied pelagic populations (Sourria 1994), thus showcasing the intricate interplay among different species and the complex oceanographic conditions they depend upon.

Tropical and subtropical regions are characterized by relatively low phytoplankton concentrations all year round and high concentrations of cyanobacteria, bacterioplankton, and ciliates during the warm season (Cepeda et al. 2020). Below 40°S, SCZ, MC,

and ACC make up a remarkable marine frontal system in the SAO and SO (Acha et al. 2020). These oceanographic structures support an intense unidirectional flow of ocean currents from the Pacific to the Atlantic Ocean through the Drake Passage (Thompson et al. 2012) and contribute to the continuous supply of cold, nutrient-rich waters and resources for pelagic copepods (Acha et al. 2020), with food size and quality favoring the occurrence of large copepods in this region. Overall, the evidence suggests that the deviations or exceptions in copepod size patterns along the latitudinal gradient, mainly from subtropical to temperate latitudes, might be the result of successful energetic inputs of constant and abundant resources at the locations of the above-mentioned oceanographic structures.

## Ecological drivers

Coexistence and adaptations of several sizes and trophic behaviors are associated with life history tradeoffs (Atkinson 1998). In the BC domain, the environment is generally more stable, and the microbial-based production is an important fuel for food webs. Small-sized omnivorous-herbivorous copepods, such as Clausocalanidae, Paracalanidae, and Oithonidae, can feed on smaller particles than those
<figure><img src="image_8.png" /><figcaption>**Fig. 6.** Mean body size (ESD mm) of copepod families along the oxygen (mg L⁻¹) gradient in the South Atlantic and Southern Ocean (13°S–64°S). Solid lines represent the fitted values (± 95% CI, colored shading) predicted for each family using GLMM models. The corresponding *p* values, denoting statistical significance, are indicated at the top left corners: \* *p* < 0.1; \*\* *p* < 0.05; \*\*\* *p* < 0.01; \*\*\*\* *p* < 0.001. Please note that the y-axis scale varies among the families due to their different body size ranges.</figcaption></figure>

ingested by larger copepods, whereas Oncaeidae can exploit
nutrient-rich marine snow and floating substrates, playing rele-
vant ecological roles in channeling the energy of the microbial
components into the classical food web (Turner 2004).

In warm oligotrophic conditions, greater specialization, such as carnivory, is evident in medium-sized Corycaeidae, and large-sized Euchaetidae, Candaciidae, and Sapphirinidae (Woodd-Walker et al. 2002; Teuber et al. 2019). Although their narrow latitudinal range indicates that they are restricted to the specific environmental niches where they are prevalent, in the tropics, their significance to the environmental variables analyzed suggests they play a meaningful role in response to shaping the copepod community structure through biological interactions, such as predation and competition, and contribute to the stability of ecosystem processes (Woodd-Walker et al. 2002). They are rapidly and continuously metabolizing food for growth and reproductive processes (Teuber et al. 2019). Carnivorous families are associated with tropical oligotrophic conditions, whereas current-feeding herbivores are associated with more productive and seasonally varying conditions in the SAO (Becker et al. 2021), pointing to the potential for increased predation at low latitudes. Indeed, the dominance of larger *Calanus* species at

high latitudes due to reduced importance of visual predators in
the Arctic (Kaartvedt 2000) supports the idea that the larger size
of some species in colder climates may also be a response to
decreased predation pressure.

Polar copepod assemblages are characterized by two principal life history strategies that allow them to adapt to varying food availability and seasonal changes and contribute to their success in the Southern Ocean (Atkinson 1998). The generalist feeding strategy is exemplified by the omnivorous Oithonidae, which includes species like *Oithona similis* feeding throughout the year on a wide range of food sources. In contrast, another strategy relies on lipid storage by diapause stages. Herbivorous Calanidae species, such as *Calanoides acutus*, experience a brief reproductive period during the summer months and subsequently enter diapause at depth to survive the winter (Atkinson 1998). This dichotomy of strategies underscores the complex interplay between species' adaptations and the dynamics of the Southern Ocean ecosystem (Woodd-Walker et al. 2002).

Temperature is generally explained as the main driver,
either for having direct effects on developmental rates or
metabolism, or due to its indirect effects on either the
duration of seasonal productivity or oxygen solubility (Verberk et al. 2021). However, the thermoregulatory consequences of being large are not the only hypothesis responsible for larger bodies in colder climates. In fact, Bergmann's rule may be linked to the decreasing latitudinal gradient of species diversity from the equator to the poles. Lower diversity means reduced interspecific interactions, including competition, a condition that may favor the size increase of smaller species (Iriarte et al. 1990). According to Corona et al. (2021), seasonal changes in copepod body size may reflect density dependent mechanisms via competition for food and/or intraguild predation in periods when the food to zooplankton biomass ratio is low.

## Climate drivers

Equatorial biodiversity is at risk due to decreasing species richness, which suggests that the equator is already too hot for some species to survive (Chaudhary et al. 2021). With continued warming, further low latitude declines in the number of species are expected (Chaudhary et al. 2021). Over the past few decades, a greater latitudinal shift in zooplankton body size was driven by a strong decline in copepod populations across the North Atlantic, owing to greater warming conditions in the northern hemisphere (Beaugrand et al. 2010; Cornwell et al. 2020).

Despite uncertainties about the drivers of copepod body size decline, some species have proved to be more resilient. For instance, *O. similis* has maintained stable populations over the past three decades in the western English Channel (Cornwell et al. 2020). Our study in the SAO and SO regions indicates that certain small copepod families, including Oithonidae, Oncaeidae, and Paracalanidae, are ubiquitous and have generally abundant populations, showing little or no variation in body size across latitudinal gradients. This remarkable characteristic suggests that these copepod families might possess a higher degree of resilience to climatic variability. These families may therefore emerge as “winners” if smaller taxa replace larger ones due to warming-induced decrease in median body size (Campbell et al. 2021; Benedetti et al. 2023).

Bergmann's rule suggests that phenotypic plasticity, rather than genetic differences, accounts for much of the latitudinal variation (Geist 1987). Copepods with higher thermal limits or copepods that can survive at higher temperatures are less able to acclimate to temperature changes within their life spans (Sasaki and Dam 2021). Projected environmental changes indicate an increase in the number and habitat area of copepod carnivorous species due to poleward expansion, at the expense of herbivorous copepods at high latitudes (McGinty et al. 2021). Therefore, these warm-adapted, low-latitude populations are more vulnerable to warming as they already experience temperatures near their thermal maxima and lack the ability to respond to increases in temperature through phenotypic plasticity (Vinagre et al. 2016).

## Conclusion

The present study reveals that body size latitudinal patterns exhibit greater complexity than previously thought, extending beyond the constraints of Bergmann's rule. This insight challenges conventional ecological paradigms, highlighting the role of oceanographic features in strengthening the latitudinal patterns of copepod body size distribution in the SAO and SO during the austral summer, primarily driven by temperature and the varying life history strategies of copepod families. Neglecting family-specific differences in body size latitudinal gradients may lead to underestimating the actual potential impacts of warming. Examining the size distribution patterns of copepod families across other oceanographic regions would contribute to better understanding whether similar ecological adaptations underlie these patterns in different western boundary currents worldwide. As our planet and ocean warm, gaining a comprehensive understanding of how keystone copepod life history and body size latitudinal patterns adapt to changing temperatures will be critical for predicting ecological shifts in marine ecosystems.

## Data availability statement

The dataset on copepod family abundance, biomass, and size distribution is currently being processed in line with the AtlantECO project's grant agreement and data management plan. Once processed, the dataset will be made publicly available through the AtlantECO-BASE platform at: www.data.up.ethz.ch/shared/AtlantECO/BASE/.

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## Acknowledgments

We would like to express our gratitude to the Brazilian Navy, the crew, and the scientific teams of the MCT-II and *Tara* Oceans expeditions for their invaluable technical assistance and support during fieldwork. We extend our thanks to the EMBRC Quantitative Imaging Platform (PIQv) and the CCPv collection for the scanning of the samples and access to the *Tara* Oceans samples, respectively. We would also like to thank Amanda Elineau for the access to the PIQv platform at the Institut de la Mer de Villefranche sur Mer (IMEV) and the CCPv collection. ECB acknowledges the support from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) under grant agreement no. 88882.438735/2019-2101, which also funded ASF's research stay at the Laboratoire d'Océanographie de Villefranche-sur-Mer under Finance Code 001. Furthermore, the research leading to these results has received funding from the European Union's Horizon 2020 research and innovation programme, project ASSEMBLE Plus (Grant no. 730984), and the project AtlantECO (grant no. 862923). This work was also supported by EMBRC-France, whose French state funds are managed by the Agence Nationale de la Recherche (ANR) within the "Investissements d'Avenir" program (PIA) under reference ANR-10-INBS-02, and the project OCEANOMICS (ANR-11-BTBR-0008). ASF benefited from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) grants (312644/2013-2 and 311994/2016-4). Open access publishing facilitated by Istituto Nazionale di Oceanografia e Geofisica Sperimentale, as part of the Wiley - CRUI-CARE agreement.

## Conflict of Interest

The authors declare no conflicts of interest.

Submitted 12 October 2023

Revised 10 April 2024

Accepted 03 September 2024

Associate editor: Maarten Boersma