Climate-Driven Changes in Freshwater Inputs to a northern Patagonia Fjord and overfishing of wild mussel seed could threaten Chilean mussel farming

doi:10.21203/rs.3.rs-4477580/v1

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Climate-Driven Changes in Freshwater Inputs to a northern Patagonia Fjord and overfishing of wild mussel seed could threaten Chilean mussel farming

https://doi.org/10.21203/rs.3.rs-4477580/v1

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Chile is the first world exporter of farmed mussels with an annual harvest about 400000 tones, such production is based on the capture of wild seed which availability may be threatened by climate change and overfishing. Climate change-induced decreasing trends in annual precipitation, which increases water column salinity and this could be affecting the vertical distribution of mussel populations in fjords. In the Reloncaví Fjord, Chile, the observed changes in precipitation reduce the freshwater inputs, leading to potential shifts in the habitat and distribution of the economically significant Chilean mussel (Mytilus chilensis) and a competing species, Aulacomya atra. This research analyzes mussel beds' vertical dynamics in relation to changing environmental conditions, including freshwater inputs, salinity, and hydrological regimes in an exploited fjord for mussel seed collection. The findings suggest that decreasing trends in precipitation could result in increased surface salinity, reducing M. chilensis beds while favouring A. atra, with negative consequences for wild seed collection therefore threatening the Chilean mussel farming industry, projecting socio-economic impacts for small-scale aquaculture. Also, this study describes the increasing fishing pressure for wild mussel larvae and suggesting joint effects which are not possible to untangle with the present information and represents a key challenge for the design of adaptation measures for climate change. Therefore, this study emphasizes the need for better monitoring of mussel beds along with seed production and oceanographic conditions as well as improving aquaculture practices that reduce unnecessary pressure on mussel beds through seed collection in the face of changing environmental conditions.

Reloncaví fjord

Mussel beds

Salinity changes

Hydrology

On a global scale, the current accelerated climate change has significantly modified the ranges and timing of precipitation (Cai et al. 2020; Ebi et al. 2021). In mid-latitudes, such as the case of south-central Chile, present changes and future projections point to significant decreasing trends in annual precipitation amounts, with changes in the form (less snow, more rain), intensity and timing of precipitation events (Garreaud, 2018; Vicuña et al. 2011). These types of alterations are particularly evident in northern Chilean Patagonia (41ºS - 47ºS), where precipitation records indicated decrease rates in the past 30 years (Cai et al. 2020).

This interannual trend has been linked to the weakening of westerly winds, a condition that during the last decades has been associated with the transition to the positive phase of the Southern Annular Mode (SAM) index (Morales et al. 2020; Villalba et al. 2012). Similarly, during years dominated by El Niño conditions, precipitation values recorded in the northern part of the Chilean fjords and channels system (NCFCS) have tended to be significantly lower than historical ranges, especially in the summer and autumn periods (Garreaud 2018; Lara et al. 2008; León-Muñoz et al. 2018). On the other hand, the alteration of precipitation patterns and to a lesser extent the moderate increase in air temperature has also generated alterations in the ranges and temporality of the natural flow regime described for the rivers of this macro-region (Aguayo et al. 2021).

As a whole, the observed changes in precipitation and natural flow regime have indicated, on average, lower freshwater inputs to the coastal system of northern Chilean Patagonia, whose water column is characterized by a marked pycnocline, largely explained by changes in salinity that are highly dependent on freshwater inputs from the rivers (Pickard 1971; Pickard and Stanton, 1980; Silva et al. 1995; Valle-Levinson et al. 2007).

For intertidal and shallow marine and estuarine biological communities, such alterations trigger changes in the distribution and abundance of fish, benthic invertebrate, and plant species (Barth et al. 2007; Cochrane et al. 2009; Harley et al. 2006; López-Gappa, 2022; Roessig et al. 2004). These changes can trigger cascading effects including reduced marine biomass and diversity, particularly at higher trophic levels (Horta et al. 2022; van Leeuwen et al. 2021; Zunguza et al. 2022), also affecting the economy of coastal human communities that depend on fisheries.

In this regard, mussels such as Aulacomya atra and Choromytilus chorus from the NCFCS are fished for direct consumption and local demand (Carranza et al. 2009). On the other hand, the Chilean mussel Mytilus chilensis is produced for export, so its seeds are collected for aquaculture, taking advantage of its life cycle that alternates between a planktonic larval phase and a benthic adult phase (Buzeta et al. 1988; Chaparro and Winter, 1983; Ramorino and Campos, 1983). Thus, seeds are captured on settling ropes and fattened for an annual production of approximately 400,000 t of farmed mussel (Molinet et al. 2021, http://www.sernapesca.cl/informes/estadisticas). Such farming practice is known as capture-based aquaculture (Lovatelli and Holthus, 2008) and the captured wild mussel seeds sustain the second most important aquaculture production in Chile, and the largest global export of farmed mussels (https://amichile.com/quienes-somos-cloned-2635/).

The characteristics of some estuarine systems allow the distribution and "vertical isolation" of M. chilensis larvae settlement in the suspended ropes (with respect to competitors such as A. atra), allowing producers to access almost 100% Chilean mussel seed in their ropes (Molinet et al. 2021; Segura et al. 2022). Adult populations of mussels are, spatially structured in subpopulations according to habitat type (Hanski and Gilpin, 1991; Roughgarden et al. 1985) and occupy defined spaces on the seafloor of estuaries between the mid intertidal and ~3-20 m depth in the subtidal zone (Roa-Ureta et al. 2015; Viviani 1979).

Considering the vertically stratified distribution of mussels in estuarine systems, Molinet et al. (2015) proposed this attribute to study factors influencing contraction and expansion dynamics of mussel subpopulations along the bathymetric gradient (following Orensanz and Jamieson 1998; Orensanz et al. 2006). Furthermore, because their life history and socio-economic relevance, mussels are ideal study units to assess at bounded spatial scales, the effect of environmental stress on their distribution in the NCFCS (Caza et al. 2016; Molinet et al. 2015). Furthermore, as previously mentioned, the NCFCS, where all fishing and aquaculture of M. chilensis is concentrated, shows a marked decrease in freshwater inputs via direct precipitation and river inputs (León-Muñoz et al. 2021), a disturbance that towards the middle and end of the century could even imply between 10 and 30% less precipitation (Aguayo et al. 2021). In this regard, we hypothesize that the ongoing declining trends in freshwater inputs, by affecting the vertical stratification of the coastal water column, may impact the habitat of mussels, restricting the optimal environment for M. chilensis, and expanding the vertical distribution of A. atra towards shallower habitat. Such changes would respond to the A. atra preference for higher salinity water compared to M chilensis which has a wide salinity tolerance range but is less competitive using space and more vulnerable to predation (Burzio et al. 1997; Curelovich et al. 2016; Viviani 1979). The described potential modification of the spatial distribution and abundance of both species could jeopardize the capture and quality/purity of seed used by the M. chilensis mussel industry, in turn generating strong socio-economic repercussions/conflicts for small-scale aquaculture (SSA)(Fernández et al. 2018; Figueroa and Dresdner 2016). In addition to the potential impacts of climatic variability on the Chilean mussel beds, the intensive harvest of their seed for aquaculture could also be a threat for the permanence and sustainability of mussel beds and therefore of seeds. The interaction of climatic forcing and fisheries and their joint effects on marine resources and biodiversity is one of the major global knowledge gaps requiring high priority to better planning and management of marine resources. Furthermore, although there is plenty of literature addressing climate change on mussel farming (Froelich et al. 2018, 2020) most studies use modeling and simulations (e.g. Fuentes-Santos 2021) to project impacts while there are very few field assessments providing evidence. This study is an initial attempt to collect field data of climatic variability and trends together with fishing pressure on mussel seed for aquaculture.

Considering current and future drought trend scenarios, here we assess the vertical contraction and or expansion of M. chilensis and A. atra beds in Reloncaví fjord (41,5ºS), the northern most fjord of the NCFCS and main source of seed for M. chilensis aquaculture during the past decade. We also estimate an indicator of fishing pressure to advance our understanding of the complexity of events and impacts associated to climate change and direct human pressure. This could allow to forecast future trends and to advance some climate change adaptation measures for mussel farming in Chile.

2.1 Study area

The Reloncaví Fjord (41° 44' S and 72°32' W), has mussel beds in practically all its extension, and it is estimated that around 60% of the seed of M. chilensis demanded by Chilean mussel farming are obtained here (Segura et al. 2022). The fjord space is highly fragmented for the following uses: i) aquaculture concessions for mussel and salmon farming, ii) management and exploitation areas of benthic resources (MEABR), iii) areas with special permissions for mussel seed collection (Fig. 1), as well as iv) fishing in open access areas.

This fjord is a highly stratified system given its morphology (width ~3-5 km, length 60 km, maximum depth ~450 m) and high freshwater inflows (Fig. 1) (Valle-Levinson et al. 2007).

The main freshwater tributaries in this system are the Petrohué (280 m³/s), Cochamó (100 m³/s) and Puelo (650 m³/s) rivers, in addition of numerous other basins of smaller size and flow (Fig. 1) (León-Muñoz et al. 2021; https://chonos.ifop.cl/mosa/?domain=chiloe ). Depending on these conditions, in the upper fraction of its water column (0 - 20 m depth) there are strong spatial-temporal variations in temperature (9-18ºC) and salinity (2-33) (Castillo et al. 2015; Daneri et al. 2009; Molinet et al. 2015; Pickard, 1971). Another relevant characteristic of this fjord is the tidal amplitude, which varies between 6 to 7 m during spring tides and 5 to 6 m during neap tides (Valle-Levinson et al. 2007). Primary productivity of the Reloncaví Fjord is highly seasonal, with higher biomass values in spring (September) and autumn (March-April) (Iriarte et al. 2007; Lara et al. 2016).

The sampling sites were distributed considering the spatial division of the fjord made by Daneri, et al. (2009), who identified 4 sections according to their hydrodynamic and morphological characteristics: “Boca” at the mouth of Reloncavi fjord, two areas in the central gorge of the fjord; “Marimelli” and “Puelo”, and Cochamó, at the head of the fjord (Fig. 1). In each section, 2 to 4 benthic sites were sampled (Fig. 1, Appendix, Table A).

2.2 Collection of information

2.2.1 Estimation of seed harvesting pressure

Taking advantages of mussels' ability to settle on filamentous substrates (Fuentes and Molares, 1994; Tamarin et al. 1976), mussel seed collection takes place using a double or single long line system which sustain lines of ropes with a weight on the rope deeper end (Molinet et al. 2021; Segura et al. 2022). Ropes, approximately 4 m length and separated by 0.2 m, are installed on the long lines to collect seeds between 1 and 8 m depth along the fjord.

To have an indirect evaluation of the fishery intensity on M. chilensis seed, we used a long line pressure index (LPI) for the previously defined zones (Boca, Marimelli, Puelo and Cochamo). This was obtained from the ratio between the total length of long lines that collect seeds per zone and their corresponding shoreline length. To do this, the long lines installed in the Reloncavi Fjord were georeferenced and measured, and also the coastline for each zone was estimated, using images available from Google Earth between 2005 and 2020. These images have a resolution that allows identifying the length of each long line. The images were exported to ArcGIS 9.3 in kml format, where the information was displayed, the number of long lines was counted, and the length of each cultivation line was calculated. The type of long lines (double or single) installed was confirmed during the sampling activities. Finally, the long lines and shorelines were quantified by zone along the fjord (Boca, Marimelli, Puelo, Cochamó).

2.2.2 Variation in vertical distribution of M. chilensis and A. atra

The vertical distribution (~20 to 0 m depth) of M. chilensis and A. atra populations was studied at 12 to 14 sampling sites distributed along the Reloncaví Fjord (from the head to the mouth of the fjord), in three periods (2015, 2020 and 2022).

At each sampling site, 3-6 video transects (25 - 35 m long) were recorded along cross-shore gradients, in vertical profiles from 12-15 m depth to the upper limit of the intertidal (Table 1), which were separated by distances of 20 to 50 m. In each of these transects, videos were taken using a Seaviewer underwater camera (900 and 6000) and a Gopro camera. This method allows us to confidently identify individuals >20 mm in length.

Both cameras were mounted on a stainless-steel sled (0.35 m high; 0.3-0.5 m wide), at the base of which a 0.1 m accurate depth gauge (in the camera's field of view) was installed. The sled was kept perpendicular to the bottom with the support of a diver, who verified the boundaries of M. chilensis beds. During sampling at low tide, the sled was towed through the intertidal to the identified barnacle’s boundary, estimating the height between sea level and the video-transect boundary.

Complementarily, in each transect a sample was collected in the intertidal and another in the subtidal (using a 0.25x0.25 m quadrat) to count and measure the shell length (SL) of M. chilensis specimens. We identified individuals recruited during the previous year, as those whose SL was less than 26 mm (Asencio, 2015, and no published data from C. Molinet). Also, we recorded individuals larger than 39.7 mm SL, size at which 50% of female are sexually mature (SL₅₀), following Molinet et al. (2016).

2.3. Image processing

To classify the type of substrate (as an indicator of sampled frame) and to quantify and identify the mussel species present, freeze-frames were taken in 30-50 cm wide quadrats. The recording time (hour: minute: second) and depth were recorded for each frame. The geographic coordinates of each sampled frame were obtained by aligning the video recording time and GPS recording time. From the processed images, a database was elaborated considering video number, sector, depth, species observed, their abundance, and coverage.

The processing of the video-transects was validated by an expert observer, who reviewed 10 seconds of each video. In cases where the review had objections, the video was reviewed again paying attention to the sources of error (e.g. sampler, video quality, sector, other). The application of this methodology was done assuming that the observed density of mussels could be underestimated because these organisms can be arranged in layers, where even the juveniles adhere to the byssus of the adults, so the density estimated is considered a proxy of the real density according to this image recording methodology (Molinet et al. 2015).

2.4 Puelo River flow and water column salinity records

To characterize the monitoring sites through the study periods, salinity data of the water column of the Reloncaví Fjord and the flow of the Puelo River, the only tributary course with continuous records of this system, were collected and systematized.

The flow data of the Puelo River were obtained from the repositories of the Chilean Water Directorate (DGA), specifically from the Carrera Basilio gauging site, which is located upstream of its outlet in the Reloncaví Fjord (https://dga.mop.gob.cl/Paginas/default.aspx).

Salinity was obtained from sampling sites of the Fisheries Development Institute (IFOP), who has been recording salinity profiles (CTD Seabird 19), with approximately monthly frequency, at 3 points in the Reloncaví Fjord (one site in the Puelo area and two sites in the Marimelli area (north and south), (Fig. 1C) since 2013 (Segura et al. 2022). In addition, the Caicura site was considered as a reference since it is located near the river discharge to the Reloncaví Fjord (Fig. 1 C).

Considering that M. chilensis and A. atra beds are distributed between 0 and 20 m depth, only the layer between 0 and 20 m depth of the CTD records was considered for this analysis.

2.5. Data analysis

Since M. chilensis is distributed in the intertidal and subtidal, the first step of the data analysis was to standardize the depths of the surveys carried out during 2015, 2020 and 2022. For this, a reference of the highest tide level (HTL) was defined, correcting the time and height for the Reloncavi Fjord relative to the Puerto Montt Pattern Port (SHOA Pub.9000, www.shoa.cl; https://www.ioc-sealevelmonitoring.org/). The depth of each frame of the analyzed video-transects was referenced to HTL using the following formula:

Frame depth= Depth₀+(HTL-TLS)

where: Depth₀ is the depth or height observed in the sampling, TLS is the tide level at the time of sampling (according to the tide table) and HTL, as mentioned, is the reference level of the highest tide.

Once the sampling depths were standardized, the depth variation of the mussel beds was analyzed, considering in each vertical profile and video-transect the presence (at least 1 mussel) /absence of the species A. atra and M. chilensis. For each video-transect, site and species, the average, minimum (upper limit referred to the HTL, with at least a mussel) and maximum (lower limit referred to the HTL, with at least a mussel) depths were estimated.

The variation of the three depths (minimum, average and maximum) was evaluated using linear mixed models and generalized linear mixed models, when the linear models did not meet the assumptions of normality and homoscedasticity of the residuals (Crawley, 2007; McCullagh and Nelder, 1989; Venables and Ripley, 2002). Year, area, species, and density (Individuals/m²) were used as fixed effect predictor variables. The sampling site and zone (Boca, Marimelli, Puelo, Cochamo) variables were evaluated as random effects because their hierarchical structure. To analyze the sources of variation, a type II ANOVA was applied, considering that the samplings were unbalanced (different number of transects per year, zone and site). In addition, the effect of the Long lines pressure index on the variation of the minimum, average and maximum depth of the M. chilensis and A. atra beds was analyzed, using linear and non-linear models (Crawley 2007). For this analysis we considered the LPI of 2014, 2018 and 2020, which were compared with the average, minimum and maximum depth of mussels in 2015, 2020 and 2022, respectively.

To identify salinity temporal trends, we used the data series available from IFOP (4 sites, between 1 and 20 m depth) between 2013 and 2022, the linear trend of mean, minimum and maximum salinity values were analized (Crawley 2007). The Puelo River flow data series for the same period was also explored.

The Akaike information criterion (AIC) (Akaike 1974; Burnham and Anderson 2004) was used to select the most informative models on the variation of the average, minimum and maximum depth of the A. atra and M. chilensis beds. All analyses were performed in R 4.3.0 (The R Development Core Team 2024), making use of the following libraries: car (Fox and Sanford 2010), nlme (Pinheiro et al. 2013), MASS (Venables and Ripley 2002), lme4 (Bates et al. 2015), ICcmodavg (Mazerolle 2023).

3.1 Long line pressure index (LPI)

The availability and quality (e.g. cloud coverage) of Google Earth images allow us to estimate the length (km) of long lines by zone for the years 2005, 2012, 2014, 2018 and 2020. A systematic increase in the installed capacity for seed collection in the Reloncavi Fjord was evident through time in the four zones. In Marimelli zone the seed collection capacity increased the most, going from approximately 28 km of long lines in 2015 to more than 70 km of long lines in 2020 (Fig. 2A). The Boca zone was the only one where the length of long lines slightly decreased between 2018 and 2020.

On the other hand, the LPI obtained shows that in 2014 the four studied zones had a ratio close to 1:1 (Fig. 2B). In 2018 all four zones exceeded the 1:1 ratio, while in 2020 this ratio was lower in Boca and increased to approximately 1.5:1 in the other three zones.

Only the maximum depth of M. chilensis beds was affected by LPI (Appendix Fig. 8 and Table B), showing a negative non-linear effect on it, such that increased LPI increases the maximum depth of M. chilensis beds. Depth of A. atra beds was not affected by the LPI.

3.2 Freshwater inputs and water column salinity.

The flow time series indicated a reduction in freshwater input from the Puelo River to the Reloncavi Fjord especially from 2010 onwards. Under this condition, mussel bed sampling years were representative of contrasting hydrological scenarios. During 2015, the volume of water contributed by this river was above the mean of the amounts dated between 1993 and 2022. In contrast, the years 2020 and 2022 corresponded to years with freshwater inputs below the average of the last three decades (Fig. 3A). The years 2020 and 2022 are in the context of a period of 4 hydrological years under the average flow values of the Puelo river (2019-2022), a condition different from that evidenced for the years preceding 2015. At the hydrological regime level, the late autumn and winter months of 2015 registered positive anomalies with respect to the average regime (1993-2022) (Fig. 3B). Later this condition changed, observing lower freshwater inputs in the spring and summer periods. On the other hand, in the winter and summer periods of 2020 and 2022, freshwater inputs from the Puelo River to the Reloncaví Fjord showed negative anomalies while showing positive anomalies in autumn (2020) and spring (2022) (Fig. 3B).

Upstream, in the water column of the Reloncaví Fjord (Puelo), the monthly salinity recorded between 0 and 20 m depth varied between 4-30, with an increasing gradient towards the mouth of the fjord (Marimelli) and the surrounding area of the Reloncaví Sound (Caicura; Fig 1 and 4). During the period 2013 - 2022, the four sites sampled by IFOP recorded a linear monthly trend (from 8 to 11 annual records) of significant increase in minimum salinity of approximately 5 (Fig. 4, Appendix Table C). The mean salinity recorded between 0 and 20 m depth varied between 22 and 30 (Fig. 4A and D, Appendix Table C), with a significant linear trend detected only at Caicura (outside the fjord, Fig. 4D). Finally, the maximum salinity recorded between 2013 and 2022, between 0 and 20 m depth, varied between 30 and 34, resulting in a significant linear trend to increase at the Marimelli north and south sites and at Caicura (Fig. 4B-D, Appendix Table C).

3.3 Vertical distribution of mussel beds

In the years 2015, 2020 and 2022, 82, 38 and 58 video-transects were registered, respectively, at the 12-14 sampling sites distributed in the 4 study areas of Reloncavi Fjord (Fig. 1). The vertical distribution and density of the mussel species evaluated varied along the fjord and between sampling years. Thus, while M. chilensis predominated between 3 and 10 m, A. atra predominated between 6 and 18 m depth (Fig. 5). In both species, a pattern of deepening distribution was observed towards the head of the fjord (Puelo and Cochamó sectors; Fig. 5).

3.3.1 Average depth

On a temporal scale, the M. chilensis belt was narrower during 2020 compared to what was observed in 2015 and 2022 (Fig. 5, Appendix Fig. 9). In the sampling years, the density of M. chilensis varied between 1 and approximately 1,000 ind/m2, with the highest density of this species being recorded during 2020 and at the sites at the mouth of the fjord, while the lowest density was recorded in the 2022 samples. On the other hand, the density of A. atra ranged from 1 to approximately 500 ind/m2, with denser sampling sites during 2015 (Appendix Fig. 9).

The average depth of the M. chilensis beds varied between 3 m (Puelo sector, year 2020) and 11 m (Cochamó sector, year 2022), with decreasing average depth during year 2022 towards the Boca and Marimelli sectors. In the Cochamó sector, the average depth of the M. chilensis beds was greater during the year 2022 (Fig. 6C, appendix Fig. 9). Meanwhile, the average depth of A. atra. varied between approximately 8.5 m (Boca, 2022) and 15 m (Puelo 2015), showing a pattern of variability similar to that described for M. chilensis (Appendix Fig. 9A).

Statistically, the most informative model to explain the average depth variation of M. chilensis and A. atra beds was a mixed GLM model of the Gamma family that considered species, zone and year as fixed effects and sampling site as random effect (Appendix, Table D). On a spatial scale, between the Marimelli, Puelo and Cochamó zones, the depth of the beds showed no significant differences, while in the mouth of the fjord the beds of both species were shallower compared to Puelo and Cochamó (Appendix, Table E). The average depths of M. chilensis and A. atra beds were shallower between 2015 and 2020 and between 2015 and 2022, although no statistical differences were observed between 2015 and 2022.

As a result, the average depth of the M. chilensis beds predicted by the model ranged between 6.2 m (Boca, 2022) and 9 m NRAM (Cochamó, 2022), while for A. atra the predicted average depth ranged between 10.1 m (Boca, 2022) and 13.5 m (Cochamó, 2022) (Fig. 6, Appendix Table H).

3.3.2 Minimum depth

The minimum depth of M. chilensis ranged from approximately 3 m (Boca, 2022) to ~8 m (Marimelli, 2015). In seven of the 12 sites where M. chilensis beds were present the average minimum depth decreased in 2020 and 2022, relative to 2015 and this was more evident towards the mouth (Boca zone) of the fjord (Appendix Fig. 9B).

For A. atra beds, the minimum depth ranged from approximately 6 m (Boca, 2022) to approximately 14 m (Puelo, 2015). Nine of the 12 sites sampled showed decreases in minimum depth relative to 2015 and only in the Cochamó area there was an increase in minimum depth for this species (Appendix Fig. 9B).

The most informative model to explain the variation in the minimum depth of the presence of M. chilensis and A. atra was the one that considered species, zone and year as fixed effects, and site as a random variable (Appendix Tables D and F). Multiple comparisons between zones showed that the minimum depth of the beds was different between Boca and Puelo, and Boca and Cochamó, while temporally differences were observed between 2015 and 2020 and between 2015 and 2022 (Appendix Table F).

Model-predicted minimum bed depth for M. chilensis ranged from 4.3 m (Boca, 2022) to 6.9 m from HTL (Cochamó, 2015) (Fig. 6 A-C), while for A. atra the predicted minimum depth ranged from 8.3 m (Boca, 2022) to 13.4 m (Cochamó, 2015) (Appendix Table H).

3.3.3 Maximum depth

The maximum depth of M. chilensis beds varied between approximately 7 m (Boca, 2020) and 13 m (Cochamó, 2022), with a decrease in maximum depth observed only at Boca while in Puelo and Cochamó the maximum depth increased (Appendix Fig 9C). The maximum depth of A. atra beds was more heterogeneous than that observed for M. chilensis, with a decrease in maximum depth at Boca and Marimelli and an increase at Puelo and Cochamó, although less evident than the increase in maximum depth observed for M. chilensis (Appendix Fig. 9C).

The most informative model to explain the variability of the maximum depth of M. chilensis and A. atra beds in Reloncavi Fjord was the one that considered species, area and year as fixed effects (Appendix Table C and G). The multiple comparisons analysis showed greater differences between the Boca and Puelo zones and between Marimelli and Puelo, while temporally differences were observed between the years 2015 and 2020 and between the years 2020 and 2022 (Appendix, Table G).

The maximum depth of the M. chilensis beds, predicted by the model, ranged between 8.1 m (Boca, 2020) and 10.7 m from HTL (Puelo, 2022), while for A. atra the maximum predicted depth ranged between 12 m (Boca, 2022) and 15.9 m (Puelo, 2022) (Fig. 6 D-F, Appendix Table H).

In summary, the values predicted by the fitted models for the average, maximum and minimum depth of the presence of M. chilensis and A. atra indicated: i) a separation between both species at ~0.5 to 3 m depth during the years 2015 and 2020 (Fig. 6A and B), while in 2022 they slightly overlap, except at the head of Reloncaví Fjord (Cochamó) (Fig. 6C), ii) the decrease in the minimum (0.2-0.6 m), mean (0.5-0.6 m) and maximum (0.4-0.6 m) depth with presence of M. chilensis and A. atra, mainly in Boca and Marimelli (Apendix Table H, Fig. 6A-C), iii) the expansion of the ranges of both species in 2022, highlighting the expansion of A. atra towards shallower depths between Boca and Puelo (Fig. 6C).

3.5 Size distribution of M. chilensis

The size distribution of M. chilensis showed a pattern of greater dispersion towards the mouth of the fjord (Boca), while towards the head of the Fjord (Puelo and Cochamó) a narrower unimodal distribution predominated (Fig. 9). In 2015 and 2020 the frequency of mature females was scarcer than in 2022. While in 2022 Mature females were well represented in the four zones identified, in 2015 and 2020 these were scarce toward the head of the fjord (Puelo and Cochamó) (Fig. 7). On the other hand, mussels until one year old were well represented in Boca during the three years studied (Fig. 7D, H and L), and more variable in the other three zones. In 2022 these young mussels were scarce toward the head of the fjord and more frequent in the mouth of the fjord (Boca zone) (Fig. 7I-L).

In estuarine systems, such as the Reloncaví Fjord, an important fraction of environmental variability is connected to freshwater discharges from rivers and direct rainwater inputs, which influence the oceanographic characteristics of the superficial water column (Lewis 1997). Additionally, changes in the stratification of the water column can influence the recruitment and survival of the benthic invertebrates (Cameron and Schroter 1980; Harrold et al. 1991; Wing et al. 2003).

Indeed, changes we are already observing in the Reloncavi fjord could have relevant consequences for mussels and biodiversity. Minimum surface salinity (0 to 20 m) in the Marimelli and Puelo zones has increased from approximately 6 to 10, just as the maximum surface salinity has increased by approximately 0.3 between 2013 and 2022, coinciding with a decrease in the mean flow of the Puelo River by approximately half in the same period. Consistent with these changes, and as predicted by the proposed hypothesis, we have observed a shallowing of both M. chilensis and A. atra beds and increased spatial overlap between the two species, suggesting that decreased freshwater inputs may be restricting the optimal habitat for M. chilensis. All these environmental changes also occur in a context of increasing fishing pressure for seed collection of this species in the Reloncaví Fjord, ecosystem providing more than 50% of the seeds for Chilean mussel (Segura et al. 2022). This is evidenced by the increase in the number of long lines and the LPI between 2005 and 2020, which also could affect recruitment, availability of reproductively mature mussels and maximum depth of M. chilensis beds. The thousands of long lines collecting seeds between one and 8 m depth could be a barrier for juvenile mussels to settle in the most superficial layers and this should be better studied and managed.

In addition, a deepening of the beds is observed from the mouth (Boca sector) towards the fjord head, modulated by the deepening of the pycnocline (Valle-Levinson et al. 2007; Molinet et al. 2015). The observed changes in the vertical distribution of mussel beds could occur on interannual time scales, through expansion processes explained by reproduction and recruitment (Oyarzún et al. 2011; Toro et al. 2004) but also by contraction due to fishing of adults mussel and their seed (Molinet et al. 2015) and, due to variations in superficial salinity (Barrett et al. 2022). The observed expansion of A. atra towards shallower areas and its greater mixing with M. chilensis suggests possible competition between both species with A. atra as a better competitor for space using its ability to produce a byssus that strongly adheres to the substrate (Burzio et al. 1997; Molinet et al. 2021), thus displacing M. chilensis. Also, increasing salinity at surface will promote the arrival of predators such as Echinodermata and Mollusca, which prefer M. chilensis than A. atra (Curelovich et al. 2016; Häussermann and Försterra 2009), all of which reduces habitat availability that has been described for M. chilensis (Häussermann and Försterra, 2009; Molinet et al. 2015; Viviani, 1979; Zaixso, 2004). Consequently, these changes threaten the intertidal and shallower subtidal rocky community structure in these systems, which is modulated by intra- and interspecific competition between organisms that adhere to the substrate, as well as predation, for example, by Echinodermata and Mollusca (Connell, 1961; Curelovich et al. 2016; Hunt and Scheibling 2001; Paine 1974; Reusch and Chapman 1997).

On the other hand, some juvenile mussels under certain conditions are able to secrete new byssus (Babarro et al 2008) and detach from the substrate and reattach to other substrates (Langley et al 1980, South et al. 2020). Therefore, it is possible that this mechanism could also contribute to interannual change in the spatial distribution of mussels, which should be studied specifically for M. chilensis and A. atra.

The size distributions of the studied Chilean mussel beds show that in all three years, individuals below 1 year old were observed towards the mouth (Boca) of the fjord, suggesting frequent recruitment in this zone compared with the other zones. Based on female maturity observed by Molinet et al. (2016), the size distribution observed suggests that M. chilensis mature females would have been frequent in Boca, while in 2015 and 2020 in Puelo and Cochamó, mature females would have been almost absent. These results could be explained by i) the higher LPI observed in Puelo and Cochamo, suggesting an overexploited system and ii) the estuarine circulation pattern in fjords (Lewis 1997; Valle-Levinson et al. 2007; Castillo et al. 2015) which could influence the accumulation of competent larvae at the mouth of the fjord. A better monitoring of seed captured by aquaculture long lines, the condition of the mussel beds and oceanographic characteristics of water column in zones studied here are key pieces to better understand the complexity of chain-effects, combining climate change and direct human intervention on mussel populations.

Considering the information available on the distribution of juvenile stages of M. chilensis and A. atra (Avendaño et al. 2011; Barría et al. 2012; Molinet et al. 2021; Molinet et al. 2017), it is also expected that the decrease in surface salinity will result in more mixed seed collection among these species, as is already occurring in other areas (Segura et al. 2022). In this sense, it is key to monitor the vertical distribution of seed collection in longlines and its relationship with changes in salinity, to advise seed mussel producers. At a practical level, and limited to the reality of Chilean mussel farming, this type of alterations should condition farmers to install increasingly shallower seed collectors, as a strategy to minimize capturing of A. atra seeds while maximizing M. chilensis seeds.

Beside the general impact in mussel aquaculture, the social and economic impacts on small-scale aquaculture (see Fernández, et al. 2018; Figueroa and Dresdner 2016), should be analyzed with a long-term horizon in order to propose mitigation measures. Since a large proportion of M. chilensis seed production comes from the Reloncavi Fjord, including small and micro-farmers, the loss of natural beds due to climate change also puts the industrial mussel farming and exports at risk (Soto et al. 2020). This is even more urgent if hydro-climatic projections are considered, which for northern Chilean Patagonia indicate a transition to a warmer and drier climate, where river inputs should tend to be lower than at present (Aguayo et al. 2019).

To address this potential risk, the first need is to continue monitoring changes in the vertical spatial distribution of mussels. This will allow progress in understanding the role of salinity changes in the water column, highlighting the need to evaluate the effects of droughts on marine ecosystems (e.g. Blanchard et al. 2008) and above all the urgency of protecting and conserving the river basins that provide freshwater and relevant nutrients, both relevant factors to maintain the natural cycles, productivity and biodiversity of these NCFCS (León-Muñoz et al. 2021). Furthermore, it is urgent to increase scientific efforts to understand the potentially additive or synergic effects of increasing salinity with the increasing fishing pressure, that is mussel seed collection, since a better management of the latter could reduce pressure on the mussel beds (Soto et al. 2020) and it could also be part of the mussel farming adaptation approach under climate change. It is also increasingly important to implement monitoring of mussel beds and oceanographic conditions in comparative marine conservation areas without mussel seed collection. Disentangling the interactions between climate change impacts and fishing impacts on marine resources is a key objective for the conservation of ocean ecosystem services including the provision of food.

Data availability

The datasets generated during and/or analyzed during the current study are available on request, with the only condition that its origin is cited.

Acknowledgments

This research was funded by the National Research and Development Agency, Chile, project FSEQ210030 and by FONDAP Project Nº 1522A0004 (INCAR). Authors acknowledge the support of the Instituto de Fomento Pesquero (IFOP) with key information to perform the analysis.

Author contributions

Carlos Molinet: Conceptualization; Data curation; Formal analysis; Investigation; Methodology; Supervision; Visualization; Roles/Writing - original draft; and Writing - review & editing

Doris Soto: Conceptualization; Funding acquisition; Supervision; Roles/Writing - review & editing

Jorge León Conceptualization; Formal analysis; Funding acquisition; Investigation; Project administration; Writing - review & editing.

Manuel Díaz: Investigation; Methodology; Project administration; Resources; Visualization.

Katherine Espinoza: Data curation; Methodology; Project administration; Validation.

Thamara Matamala: Data curation; Investigation; Methodology; Validation; Visualization.

Jorge Henriquez: Data curation; Methodology; Software; Validation; Visualization.

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Climate-Driven Changes in Freshwater Inputs to a northern Patagonia Fjord and overfishing of wild mussel seed could threaten Chilean mussel farming

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