Introduction

Coastal areas are typically productive environments that harbour a high biodiversity (Crossland et al. 2006) and attract human populations which are responsible for urban development and for industrial, port and agricultural activities (Halpern et al. 2008). Port areas are highly modified environments with heavy marine traffic and persistent dredging and piling activities that can generate cumulative negative impacts on the marine fauna, such as habitat loss, noise and chemical pollution (Grech et al. 2013; Todd et al. 2015). In the southwestern Atlantic Ocean, the Paranaguá Estuarine Complex is a world heritage site that includes one of the most productive estuarine areas in southern Brazil and an intensely urbanised port area (see Possatto et al. 2016). This estuarine complex is home to a large population (1371–2393 individuals; Domit et al. 2021) of Guiana dolphins (Sotalia guianensis, Fig. A1), an endemic coastal dolphin that is considered an environmental sentinel (Kajiwara et al. 2004; Van Bressem et al. 2009a; Lailson-Brito et al. 2010; Moura et al. 2014; Domit et al. 2021).

Throughout their distribution, Guiana dolphins are exposed to several human activities. Off the Brazilian coast, for instance, they are often threatened by vessel collision (Domiciano et al. 2016), entanglement and incidental mortality in fishing gear (Moura et al. 2014; Domiciano et al. 2016), bioaccumulation of chemical compounds (Dorneles et al. 2008, 2020; Lailson-Brito et al. 2010; Vidal et al. 2020; Manhães et al. 2021; Trevizani et al. 2021), and exposure to emerging diseases (Sacristán et al. 2018; Sanchez-Sarmiento et al. 2019; Groch et al 2020). These cumulative anthropogenic impacts may cause injuries (Domiciano et al. 2016) and health disorders, such as immune depression (Moura et al. 2014; Domiciano et al. 2016; Manhães et al. 2021), poor body condition (Reif et al. 2009; Van Bressem et al. 2009a, b; Domiciano et al. 2016), a higher prevalence of skin lesions and infectious diseases (Van Bressem et al. 2009a; Groch et al. 2014; Seade et al. 2017; Sacristán et al. 2018). Declines in individual health can affect population size and resilience (e.g. Azevedo et al. 2017). For example, in 2018, an epizootic event of cetacean morbillivirus caused emaciation and high mortality in Guiana dolphins from Rio de Janeiro state (Groch et al. 2018, 2020; Flach et al. 2019; Cunha et al. 2021). Moreover, a high overlap with fishing activities results in injury and mortality through bycatch (Azevedo et al. 2009; Domiciano et al. 2016). As a consequence, this species is classified as “Near Threatened” by the IUCN (Secchi et al. 2019) and considered a conservation priority by the International Whaling Commission (IWC) (Van Bressem et al. 2009a; Domit et al. 2021), and by the National Action Plan for Conservation of Aquatic Mammals in Brazil (Barreto et al. 2011).

In the Paranaguá Estuarine Complex, Guiana dolphins are found year-round, feeding and breeding (Domit 2010; Santos et al. 2010; Bonin et al. 2017; Moura et al. 2021), even in noisy and degraded areas. The exposure to human activities might be counterbalanced by high prey availability, as Guiana dolphins are often observed using the side of anchored ships in ports as a barrier to corral and capture fish (Domit 2010). Although apparently beneficial in the short term, the daily exposure to such environments may lead to long-term consequences, which can be manifested by disruption of behaviour (Bittencourt et al. 2017), poor body condition, and the presence of cutaneous conditions (Van Bressem et al. 2009a). The Guiana dolphins living near the port of Paranaguá a decade ago showed more cutaneous alterations than a population living in a relatively pristine area (Cananéia estuary: Van Bressem et al. 2009a). Such altered cutaneous conditions were considered indications of depression of the immunological system and increased susceptibility to infections (Van Bressem et al. 2009a; Domiciano et al. 2016).

Cutaneous alterations and body condition are often evident in cetaceans and can be effectively detected by photographing individual animals (Thompson and Hammond 1992; Wilson et al. 1999; Van Bressem et al. 2009a; Christiansen et al. 2020). Here, we evaluate the potential relationship between the health status and environmental conditions by comparing the cutaneous and body conditions of individual Guiana dolphins that use two areas within the Paranaguá Estuarine Complex: one with high anthropogenic activity surrounding a port, and another with low anthropogenic activity surrounding a conservation unit. We hypothesise that dolphins seen more often in and around the port have higher occurrence and prevalence of skin lesions and poorer body conditions than those seen more often at the conservation unit.

Methods

Study area

The study was carried out in two sectors of the Paranaguá Estuarine Complex, southern Brazil (Fig. 1A): adjacent to the Ilha das Peças island (IP, Fig. 1B; 25° 27′ S; 48° 20′ W) and surrounding the Paranaguá Port Complex (PPC, Fig. 1C; 25° 30′ S; 48° 32′ W). These sectors are continuously used by Guiana dolphins and were chosen for their differences in the diversity and intensity of anthropogenic activities with potential impact on marine life. The port, located in Paranaguá Bay, is the second-largest port in Brazil. Its sector include a ship manoeuvring stretch, mooring berths, public wharves, and wharves of liquid and flammable bulk (Soares and Lamour 2008). Dredging for maintenance or deepening of mooring berths, expansion of the port terminal and vessel traffic are continuous at port (Soares and Lamour 2008; Barletta et al. 2016). The Ilha das Peças island is part of the Superagui National Park, a federal conservation unit. Although the island sector is a protected area, it includes some aquatic anthropogenic activities such as artisanal fishing and tourism and is only 40 km far from the port (Abreu et al. 2017).

Fig. 1
figure 1

A Paranaguá Estuarine Complex (PEC), Paraná, southern Brazil, where the B Ilha das Peças (IP) and C Paranaguá Port Complex (PPC) are located. Red circles indicate sightings of Guiana dolphins in 2018 and 2019

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Data sampling

A total of 44 daily boat-based surveys were carried out between July 2018 and April 2019, alternating sectors each week. The sampling days were determined by the weather, tide condition and navigation safety. The port sector was sampled using a strip transect 11 km long and 1 km broad (Fig. 1C) whilst the island sector was sampled with a 12 km by 1 km transect (Fig. 1B). Transects were covered searching for groups of Guiana dolphins, here defined as individuals seen in proximity and engaged in the same behavioural state, which could vary from two to hundreds of individuals. The size and composition of the groups were recorded whenever an individual joined or left the group. The GPS location of the groups was taken, and behavioural states were recorded every 5 min (e.g. Baker et al. 2017). To evaluate environmental conditions in both sectors, water parameters (salinity, transparency, and temperature) were measured hourly, and tidal conditions were retrieved from local weather stations (http://ondas.cptec.inpe.br/).

Individual identification and health assessment

Upon encountering a group, sequential photographs of all dolphins were taken to record the dorsal fins for individual identification (see Karczmarski et al. 2022a, b). Natural marks observed on the dorsal fins were compared to identify individuals using a standard photo-identification protocol (Hammond et al. 1990). Animals that could not be individually identified (i.e. unmarked dorsal fin) were excluded from the analysis.

The visible body surface of the dolphins was photographed and examined for the presence of cutaneous conditions and to evaluate the body condition. For body condition, individuals were categorised as emaciated, thin or in good condition, based on the degree of atrophy of the epaxial musculature, prominence of ribs, and amount of subcutaneous fat in the nuchal region (Fig. 2; according to Pugliares et al. 2007; Joblon et al. 2014). In the “emaciated” category, the ribs are more apparent and a greater concavity can be observed in the latero-dorsal region and in the neck, due to loss of fat deposits and muscle mass; in the “thin” category, a moderate concavity can be observed in the latero-dorsal region of the animal and in the neck; in the “good condition” category, the latero-dorsal region of the body and the neck have a flat or convex appearance (Pugliares et al. 2007; Joblon et al. 2014).

Fig. 2
figure 2

Body condition categories of Guiana dolphins. A emaciated: apparent ribs, concavity below of dorsal fin with sharp dorsal edge (score 1); B thin: some degree of concavity below the dorsal fin (score 2); C good condition: rounded body (score 3)

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The cutaneous conditions were identified by comparing the images collected in the field with descriptions found in scientific articles from a systematic review of the literature (examples in Table 1; Fig. 3). Cutaneous conditions were classified in three categories of alterations: “lesions suggestive of an infectious aetiology” were possibly related to viral, protozoal, fungal and/or bacterial aetiology, such as lobomycosis-like disease (Van Bressem et al. 2007), nodules evoking lobomycosis-like disease (Van Bressem et al. 2009a), circular lesions and circular ulcerated lesions. The second category, “conditions suggestive of traumatic events of anthropogenic origin”, included scars that were possibly related to direct anthropogenic impacts, and may have led to deformity of dorsal fin and the dorsal region of the body, or linear indentations indicative of interaction with fishing nets. The third category, “anomalous pigmentation” included hypopigmentation and hyperpigmentation of the skin; the description, possible aetiology and references are detailed in Table 1.

Table 1 Description and categories of all types of cutaneous conditions found in Guiana dolphins observed in both study sectors (Ilha das Peças—IP, Paranaguá Port Complex—PPC) of the Paranaguá Estuarine Complex, Paraná, southern Brazil
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Fig. 3
figure 3

Examples of cutaneous conditions found in Guiana dolphins of Paranaguá Estuarine Complex, Paraná, southern Brazil (see Table 1)

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The prevalence of cutaneous conditions was calculated as the ratio between the number of photo-identified individuals with a given type of cutaneous alteration and the total of photo-identified individuals (Wilson et al. 1999; Van Bressem et al. 2003; Gonzalvo et al. 2015). The same ratio was calculated for the prevalence of categories of body condition. Changes on cutaneous and body conditions were recorded for individuals observed in both years.

Frequency of use of area

The use of the Paranaguá Estuarine Complex was estimated as the proportion of days that each photo-identified individual Guiana dolphin was recorded within the estuary relative to the total of sampled days (Batista et al. 2014). The frequency of use of each sector was evaluated by the proportion between the number of months each individual was sighted in each sector in relation to the total of months sampled (Rossi-Santos et al. 2007). From this frequency, individuals were classified as resident (> 50%), transient I (25–50%) and transient II (< 25%) in each sector (adapted from Moura et al. 2021).

Data analyses

The environmental parameters were compared between sectors using, when appropriate, parametric (Student’s t) or non-parametric (Mann–Whitney) tests. Fixed Kernel Density Estimation (fixed-KDE) was used to analyse space use and distribution patterns of Guiana dolphins in each sector. Distribution maps of groups of dolphins were made from the GPS locations and density results using software QGIS 3.10.2.

To investigate the relationship between health status and space use, a generalised linear model was built considering a Poisson error distribution and a log link function. The dependent variable was the total number of cutaneous conditions quantified per individual (the sample unit), and the independent variables were the study sector where the individual was sighted (port, island, both), the initial body condition category (suggestive of general health condition), and the frequency of use of the entire Paranaguá Estuarine Complex (estimated as the proportion between the number of days each individual was sighted in the entire area and the total number of days sampled). As a reference, a null model with only the intercept was built, and compared to the complete model using the Akaike Information Criterion for small samples (AICc; Burnham and Anderson 2002). The model was validated following the linear model evaluation protocol (Bolker et al. 2009), including inspection of Q–Q plots, presence of outliers, temporal and spatial autocorrelation, and plots of residuals against fitted data. Model validation was achieved with 1000 simulated model residuals using the DHARMa R package (Hartig 2020).

Results

During the 44 days of survey, 204 groups were sighted and 204 Guiana dolphins were identified, of which 52 individuals were seen in the both years. Most of these dolphins (59%) were seen exclusively around the island; 31% were seen exclusively around the port, and the remainder was seen in both sectors (10%). The groups were generally composed of adults (197/204; 97%) and rarely included calves (only 45/204; 22%). The average group size was similar in both locations: 10.22 ± 10.19 SD individuals around the island, 10.05 ± 6.90 SD around the port. Foraging was the most frequent behaviour in both the port (86.5%, 371 out of 429 events) and island sectors (77.6%, 378/487); other less frequent behaviours included displacement and socialising. The fixed-KDE maps for each sector suggested greater use of the mooring berths of bulk carriers in the port (Fig. A3a), and of the river mouth in the island (Fig. A3b). In the island, 85% (120/141) of the individuals were classified as transient II, 13% (18/141) as transient I and 2% (3/141) as resident, whilst in the port 78% (65/83) were classified as transient II, 10% (8/83) as transient I and 12% (10/83) as resident. The measured environmental conditions were not different between the sectors (salinity: t = − 1.4616, p = 0.1449, df = 303; water transparency: t = 0.1335, p = 0.8939, df = 270.73; water temperature: p = 0.6159; W = 7513).

Body condition

Combining both study sectors within the entire Paranaguá Estuarine Complex, 67 individuals were repeatedly sighted and had their initial and final body conditions scored. The period between initial and final scores for most dolphins (63 individuals) ranged between one and nine months (average = 4.0 months ± 2.5 SD), whilst four individuals had their initial and final body condition scored less than one month apart (Table S1). Nearly half of the individuals were classified as “thin” both in the initial (51%; 34/67) and in the final assessment (52%; 35/67); and about a quarter of the individuals were classified as emaciated in the initial (25%; 17/67) and final assessments (27%; 18/67); (Table 2; Table S1). Most dolphins maintained their initial body condition between the years (42%; 28/67), whilst 30% (20/67) decreased and 28% (19/67) improved their body condition score between years (Table S2).

Table 2 Number of individual Guiana dolphins with body condition scores in each study sector (Ilha das Peças—IP, Paranaguá Port Complex—PPC) of the Paranaguá Estuarine Complex, Paraná, southern Brazil
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Cutaneous conditions

In total, eight types of cutaneous conditions were identified (Tables 1, 3; Fig. 3). At least one type of cutaneous condition was observed in 68% (139/204) of the photo-identified individual dolphins in the Paranaguá Estuarine Complex, and in all 52 individuals sighted in both years. Amongst the 204 dolphins, 103 (50%) had cutaneous lesions suggestive of infectious aetiology, 15 (7%) presented conditions suggestive of traumatic events of anthropogenic origin and 92 (45%) had anomalous pigmentations. The prevalence of cutaneous conditions by year was 85% (76/89) in 2018 and 67% (112/167) in 2019.

Table 3 Prevalence of cutaneous conditions in Guiana dolphins of the Paranaguá Estuarine Complex (PEC), Paraná, southern Brazil, by study sector and year
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Amongst the cutaneous lesions suggestive of infectious aetiology, circular lesions (40%, 82/204) and nodules (21%, 43/204) were the most prevalent in both, the port and the island sectors (Table 3). Lobomycosis-like disease and circular ulcerated lesion were also observed but only in a few individuals (3%, 6/204) and (1%, 2/204), respectively (Table 3). Amongst conditions suggestive of traumatic events of anthropogenic origin, interactions with fishing nets were the most frequent for the animals of port sector (5%, 4/83) and for the animals in the island sector (8%, 12/141), respectively (Table 3). Among the category of anomalous pigmentation, hyperpigmentation of the skin was commonly observed in dolphins from the port sector (55%, 46/83) and in the island sector (43%, 60/141), respectively (Table 3).

The cutaneous conditions representing anomalous pigmentation were the most prevalent in Paranaguá Estuarine Complex in 2018 (86%) and in 2019 (50%), followed by lesions suggestive of an infectious aetiology (83% in 2018 and 71% in 2019) and conditions suggestive of traumatic event of anthropogenic origin (12% in 2018 and 8% in 2019). The most frequent skin conditions in the entire Paranaguá Estuarine Complex by year were hyperpigmentation of the skin in 2018 (73%) and in 2019 (42%), circular lesion (44% in 2018 and 44% in 2019) and nodule (33% in 2018 and 23% in 2019) (Tables 1, 3; Fig. 3).

Case study: regression of a nodular lesion

The progression and regression to complete resolution of a nodular lesion in individual #8 were recorded. This individual was sighted more often (77.78%) around the port, and was first sighted on 31 July 2018. It was photographed with a nodular lesion on 5 September 2018 and on 19 September 2018 several whitish and slightly raised skin lesions had developed on the back and close to the dorsal fin, a condition that evoked lobomycosis-like disease (Van Bressem et al. 2009a). The lesion extended multifocally to adjacent areas until 25 September 2018. On 12 November 2018, similar cutaneous nodules were observed close to the dorsal fin with white discoloration in the area. On 5 December 2018, lesions were observed close to the tail stock. On 14 January, 21 January, 25 February and 24 April 2019, the nodular lesions were no longer seen (Fig. A2).

Space use and health status

Amongst all 139 photo-identified individual dolphins that had at least one type of cutaneous condition, 74% were classified as transient II, 17% as transient I, and 9% as resident to the larger Paranaguá Estuarine Complex. The occurrence of lesions in Guiana dolphins that are suggestive of infectious aetiology, conditions suggestive of traumatic events of anthropogenic origin and anomalous pigmentation related to the overall frequency of use of the whole Paranaguá Estuarine Complex, independently of the study sector where the individuals were seen more often (Fig. 4). The generalised linear model (Lesions ~ body condition + frequency of use of entire estuary + study sector) suggested that the occurrence of cutaneous conditions increased with the frequency of use of the entire estuary (\(\beta\) = 0.06, SE = 0.0099, p < 0.001; Fig. 4A). Both the effects of body condition (thin: \(\beta\) = − 0.04, SE = 0.18, p = 0.817; good: \(\beta\) = − 0.13, SE = 0.21, p = 0.521) and location (island: \(\beta\) = − 0.23, SE = 0.21, p = 0.277; port: \(\beta\) = − 0.19, SE = 0.21, p = 0.369) were very small and not significant (Fig. 4B, C). The model had more support than the null model (∆AICc = 45.13), and showed sufficient explanatory power (adjusted R2 = 26.92%). There was no over-dispersion (observed/simulate = 0.956, p = 0.508), outliers (p = 0.343), lack of uniformity (One-sample Kolmogorov–Smirnov test, D = 0.038, p = 0.944), or temporal (DW = 1.790, p = 0.148) and spatial autocorrelation (Observed = 0.0005, Expected = − 0.0053, SD = 0.011, p = 0.605).

Fig. 4
figure 4

The predicted number of lesions (suggestive of infectious aetiology, anomalous pigmentation, and conditions suggestive of traumatic events) in individual Guiana dolphins increases with (A) the frequency of use of the Paranaguá Estuarine Complex, Paraná, southern Brazil, but it does not change between (B) body condition categories, or (C) the study sector where the individuals were predominantly seen. Ribbons and whiskers represent 95% confidence intervals

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Discussion

Guiana dolphins from the Paranaguá Estuarine Complex, including those using the port and areas bordered by conservation units, have a poor body condition and several cutaneous conditions. We detected eight types of cutaneous conditions, including hyperpigmentation of the skin, circular lesions, lobomycosis-like disease, nodules, and indications of interaction with fishing nets. Overall, this study provides baseline information on key health conditions of Guiana dolphins from southern Brazil.

Most dolphins in the Paranaguá Estuarine Complex showed poor body condition (“emaciated” and “thin”) and presented several types of cutaneous conditions (in 139 of 204 individuals), despite their different frequency of use of the port and the conservation unit areas. The lack of difference in the health conditions between dolphins using these two sampled areas may be due to the movement of dolphins throughout the entire estuary (Moura et al. 2021) and their fluid social dynamics with frequent social associations amongst individuals (Cantor et al. 2012; see also Powell et al. 2020). Guiana dolphin populations are typically composed by a combination of mostly transient and fewer resident individuals (e.g. Cantor et al. 2012; Moura et al. 2021), and most of the individual Guiana dolphins were considered transient II during this study (85% in the island and 78% in the port). In the Paranaguá Estuarine Complex, individual variation in spatial use may be related to intraspecific competition and the environmental characteristic that influence prey dynamics and quality (e.g. Santos et al. 2010; Possatto et al. 2016; Moura et al. 2021), but it can also be related to behavioural tactics and health conditions (Van Bressem et al. 2009a; Domit 2010). Recent studies suggest that dolphins more exposed to anthropogenic impacts have a greater chance of being severely affected by a viral epidemic than those less exposed (Collier et al. 2020; Manhães et al. 2021), possibly because of a depressed immune response and their poorer health. In addition, as other species of coastal dolphins, these dolphins may have skin lesions and lesions related to trauma caused by interactions with fishing nets or vessel collision (Chan and Karczmarski 2019). The effects of anthropogenic activities and habitat degradation on health conditions of coastal dolphins are evidenced in Hong Kong, China, where ~ 50% of the Indo-Pacific humpback dolphins (Sousa chinensis) have some form of skin lesions (Chan and Karczmarski 2019). Since emaciation has been repeatedly described in Guiana dolphins from Sepetiba Bay during and well before the morbillivirus epidemic (Van Bressem et al. 2007; Flach et al. 2019; Groch et al. 2020), the current poor body conditions of Guiana dolphins in the Paranaguá Estuarine Complex could be an early sign for the need of managing impactful anthropogenic activities in this region to avoid worsening the health conditions of this population in the near future.

Skin lesions with a possible infectious aetiology were relatively common in the Guiana dolphins of the Paranaguá Estuarine Complex. In most cases, these lesions were characterised by a circular shape or a nodule. Whilst the exact aetiology cannot be confirmed by visual inspection alone, these types of lesions have been associated to infection by fungi Paracoccidioides brasiliensis, Fusarium sp. and Trichophyton sp., bacteria Streptococcus iniae, amongst others (Kiszka et al. 2009; Van Bressem et al. 2009a; Yang et al. 2013). The incidence of nodules in the population decreased slightly from 33% in 2018 to 23% in 2019, but the prevalence of circular lesions remained stable from 44% in 2018 and in 2019. However, when compared to a previous assessment of this population, there was an apparent increase in the prevalence of nodules, 21% in this work from 12.6% in 2006–2007 (Van Bressem et al. 2009a), and stability of lobomycosis-like disease (2018–2019: 3%; 2006–2007: 3.9%, Van Bressem et al. 2009a). These findings suggest no significant improvement in health conditions in the population of the Paranaguá Estuarine Complex in more than a decade.

Moreover, we highlight that more recently, there has been increasing dredging activities, freshwater and sewage flow, and other environmental stressors in this area. Particularly, in 2018 a yearly dredging process was conducted which might have affect the highest levels and diversity of cutaneous conditions recorded, possibly due to the sediment suspension (Torres et al. 2009) and for making contaminants bioavailable throughout the food chain, thereby impacting the marine mammals (Grech et al. 2013; Todd et al. 2015). The prevalence of other types of cutaneous conditions was apparently low, especially when compared to other delphinid species. For instance, the prevalence of anomalous pigmentation in the skin of Guiana dolphins of the Paranaguá Estuarine Complex is low compared to bottlenose dolphins in Australia (Chabanne et al. 2012). However, we acknowledge that the short duration of these studies and the high prevalence of transient dolphins do not allow long-term inferences, highlighting the need for continuous monitoring to confirm any apparent trend in prevalence of skin lesions or any other changes in cutaneous condition of this Guiana dolphin population.

The prevalence of injuries likely caused by anthropogenic activities was relatively low, with 6% of the individuals showing scars, which is suggestive of interactions with fishing nets. However, it is possible that anthropogenic interactions are underestimated because we only evaluated non-lethal interactions. Bycatch has been a major cause of death (28/30; 93%) amongst cetaceans stranded in the same studied area (Domiciano et al. 2016). Few cases of a Guiana dolphin with scars suggestive of a vessel strike are recorded in the area (Domiciano et al. 2016; Public database: https://simba.petrobras.com.br/simba/web/). However, no evidence of collisions was observed during the present study.

Further, the lack of difference in the health conditions of dolphins using the port and conservation areas may also be due to fishing activities and pollutants sources affecting the entire estuary (Andriguetto-Filho 1993; Lailson-Brito et al. 2010; Abreu et al. 2017; Afonso and Chaves 2021; Trevizani et al. 2021). Polychlorinated biphenyls (PCBs) and polycyclic aromatic hydrocarbons (PAHs) have been detected in the sediment and in suspended particulate material close to the port and mangrove area (Combi et al. 2013; Cardoso et al. 2016). Additionally, mercury, trace elements and other pollutants have been found accumulated throughout the food chain, including in tissues of Guiana dolphins (Lailson-Brito et al. 2010; Trevizani et al. 2019, 2021; Vidal et al. 2020). The study sector around the conservation unit, although more distant from urban, port and industrial areas, is also likely to be under the influence of pollutants that spread in the aquatic ecosystem, affecting distant areas and several trophic levels of the local food web (Combi et al. 2013; Trevizani et al. 2019). Chemical contaminants were found in the sediment across the Paranaguá Estuarine Complex, even far from the polluting source (Choueri et al. 2009).

Caveats

There is considerable evidence that the visual examination of dolphin health conditions provides an opportunity to investigate how environmental conditions and anthropogenic activities may affect dolphin populations (Van Bressem et al. 2003, 2009a; Kiszka et al. 2009; Maldini et al. 2010; Fury and Reif 2012; Sanino et al. 2014; Gonzalvo et al. 2015; Powell et al. 2018; Leone et al. 2019; Chan and Karczmarski 2019). Combining visual inspection of body and cutaneous conditions can be a good proxy of cetacean and ecological health (Reif et al. 2009; Van Bressem et al. 2009a; Moura et al. 2014; Bittencourt et al. 2017; Chan and Karczmarski 2019), but there are limitations. Cutaneous alterations can also occur in cetaceans due to continuous exposure to low salinity, low temperature, or to abrupt environmental changes (Wilson et al. 1999; Duignan et al. 2020). Therefore, future studies will benefit from integrating visual monitoring with a deeper, pathological examination of cutaneous conditions to confirm their aetiology.

Similarly, although small dolphins are susceptible to changes in body mass and quick in losing bubbler mass when disturbed (Kastelein et al. 2019), body condition and bubbler thickness still provide a limited view of their overall health (Derous et al. 2020). This is because body conditions can also reflect how cetaceans interact with their physical and social environments (Wilson et al. 1999; Van Bressem et al. 2003, 2009a; Rowe et al. 2010; Leone et al. 2019; Duignan et al. 2020). For instance, body condition may also decrease due to fluctuation in prey availability or due to higher energetic investment in mating, reproduction, lactation, and parental care (Castrillon and Bengtson Nash 2020). Therefore, it is important to carry out long-term population monitoring to develop novel approaches that can improve the accuracy of the health assessment of free-ranging dolphins.

Closing remarks

This study provides information on the relationship between spatial use and health conditions of Guiana dolphins in southern Brazil, which can inform the much-needed local actions to conserve this species (Barreto et al. 2011). The results also provide support for monitoring of body and cutaneous conditions in cetaceans, as they are proxies of health conditions that may represent noticeable short-term responses to the quality of their environment and an indicator of ecological health. Assessing health markers remains a priority for long-term population monitoring because a decline in the health of individual cetaceans can translate into reduced foraging, reproduction potential, calf development and survival (e.g. Christiansen et al. 2014, 2020), and, therefore, reduced resilience against environmental changes and population vulnerability (Choy et al. 2019).