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Partial migration in diadromous fishes drives the allocation of subsidies across the freshwater-marine ecotone

Partial migration in diadromous fishes drives the allocation of subsidies across the... Anim. Migr. 2021; 8:40–55 Research Article Grégoire Saboret, Duncan J. Buckle, Alison J. King, Michael M. Douglas, David A. Crook Partial migration in diadromous fishes drives the allocation of subsidies across the freshwater- marine ecotone https://doi.org/10.1515/ami-2020-0108 P. ordensis acted as a net 42.6g biomass subsidy in fresh received April 30, 2021; accepted August 17, 2021 water, representing a retention of more than 50% of the juvenile mass at freshwater entry. Our model predicts Abstract: Migratory animals can act as cross-boundary that skipped spawning is likely to alter the allocation of subsidies sustaining ecosystem functioning, such as subsidies in diadromous species, highlighting the impor- diadromous fishes that migrate between fresh water and tant effects of individual variation in migratory behaviour seawater and carry nutrients and energy across the fresh- on fluxes of energy and nutrient at ecosystem scales. We water-marine ecotone. Frequency and timing of migration encourage future studies to consider how variation in are however highly variable within and among popula- migratory behaviour is likely to affect the direction and tions. We hypothesized that in catadromous fishes (i.e., magnitude of biomass fluxes across ecotone boundaries. diadromous fishes that grow in freshwater and spawn in Keywords: Partial migration; Skipped spawning; Cata- the sea, such as eels), the import of subsidies by migra- dromy; Marine-derived nutrients; Prey availability tory juveniles could outweigh the export of subsidies by adults due to skipped spawning migration. We used the diamond mullet Planiliza ordensis, as a model species, and determined life-history traits using a combination of length-to-age data, acoustic telemetry and otolith (fish ear stone) microchemistry. We used a mass balance approach 1 Introduction to model individual mass acquisition and allocation, and extended our model to other life-history strategies. Our Most ecosystems are recipients of allochthonous resources results showed high intra-population variation of migra- (i.e. not originating in the region where they are found), tory behaviour in P. ordensis, with few individuals migrat- such as nutrient, organic matter and prey, that enhance ing every year to spawn. We estimated that an individual in situ productivity [1,2]. Recent theoretical and empirical studies suggest that low to moderate allochthonous inputs (or ‘subsidies’) can stabilize trophic dynamics, defined as the movement of carbon, nutrients, and energy among organisms in an ecosystem [3,4]. However, depending on *Corresponding author: Grégoire Saboret, Research Institute for the the trophic levels that use the resource, trophic dynamics Environment and Livelihoods, Charles Darwin University, Darwin, can become unstable as inputs increase [5,6]. One striking 0810, NT, Australia example is when excessive inputs of allochthonous Master Biosciences, ENS de Lyon, Département de Biologie, 46 allée d’Italie, 69007 Lyon, France carbon from newly inundated riparian areas during high Department of Surface Waters, EAWAG, Center for Ecology, Evolution river flows create hypoxic conditions that can cause large- and Biogeochemistry, 6047 Kastanienbaum, Switzerland, Email: scale deaths of fish and other riverine organisms, and thus saboretgregoire@gmail.com the loss of the steady state [7,8]. Similarly, the transfer Duncan J. Buckle, Alison J. King, Michael M. Douglas, Michael M. of large amounts of organic matter from agricultural Douglas, David A. Crook, Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, 0810, NT, Australia activity into natural ecosystems can fundamentally alter Alison J. King, David A. Crook, Centre for Freshwater Ecosystems, trophic dynamics: trophic cascades can be initiated and La Trobe University, Albury-Wodonga, 3690, New South Wales, rare or uncommon species can become invasive while Australia functionally important common species decline [9]. Such Michael M. Douglas, School of Biological Sciences, The University of examples demonstrate the sensitivity of ecosystems to Western Australia, 6009, Western Australia, Australia Open Access. © 2021 Grégoire Saboret et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 License. Partial migration drives subsidy allocation  41 variation in the direction, extent and biochemical path- ambient conditions by delaying the timing of reproductive ways associated with subsidies [10]. investment until more suitable conditions occur [26,27]. Migratory animals transport vast amounts of energy It is increasingly recognised that partial migration and nutrients assimilated in body tissues or as waste can affect trophic dynamics in ecosystems [18,28,29]. For products (e.g., faeces, urine) across ecotone boundaries instance, the proportion of migrating cyprinids from lakes [11]. This holds particularly true for diadromous fishes to streams affect the predator community structure [30] and (i.e., fish migrating between seawater and fresh water, may drive the steady state of lakes by a top-down control such as salmons and eels), which connect marine ecosys- on plankton [31]. However, little is known on how partial tems and inland waters via subsidies. One iconic example migration influences the fluxes of energy and nutrients is the migration of Pacific salmons (Oncorhynchus spp.) between the freshwater and marine ecosystems. In the that subsidize streams with marine-derived biomass [12], current study, we hypothesized that skipped spawning which sustain lotic and riparian ecosystem functioning in diadromous fishes could be a main force driving the [13]. There is increasing evidence that other diadromous allocation of subsidies across the marine-freshwater fishes also act as important fluxes of energy and nutrients. ecotone. We used the catadromous diamond mullet, For instance, Engman, Kwak, and Fischer [14] have esti- Planiliza ordensis, an important prey species in riverine mated that the mass migration of tiny diadromous goby food webs of Northern Australia, as a model species. larva (~0.1g each) import a ton of marine-derived biomass We considered subsidies in the form of prey availability, per migration event to a single river because they migrate given the importance of mullets as prey for predators in by millions, representing a significant input of biomass to both environments. Analysis of otoliths (ear bones that the stream. Diadromous fishes include catadromous and act as natural record of growth and migratory pattern), anadromous species that use the freshwater and marine population surveys, and acoustic telemetry were used to ecosystems, respectively, as a growing biome and, marine elucidate individual life-history traits such as timing of and freshwater ecosystems, respectively, as a breeding migration, mortality, growth and migration frequency. We biome [15]. In addition, diadromy also includes amphi- applied our findings to estimate biomass fluxes across the dromy that can be considered as an extension of cata- freshwater-marine ecotone, and then explored our model dromy in which larva drift to the ocean instead of spawner with regards to variation in life-history traits. Specifically, migration [16]. Ontogenetically, diadromous fishes con- we explored how skipped spawning in other diadromous tribute unequally to fluxes: for example, adult Pacific fishes could affect the allocation of biomass between the salmons accumulate most of their mass in the ocean (> freshwater and marine environment. 95%, [12]) and typically weigh one-to-two orders of magni- tude more than out-migrating smolts (e.g 12g vs 5.5kg see [17]). Thus, the direction of spawning migration has been 2 Material and methods proposed as the main driver of nutrient flux, with ana- dromous and catadromous fishes expected to represent a gain and a loss of nutrients and energy for freshwater 2.1 Study species and study system ecosystems, respectively [18]. An emerging theme in research on migratory animals Planiliza ordensis (Family Mugilidae) is endemic to over recent decades, particularly with the advent of Northern Australia [32,33]. It grows to a maximum size telemetry and other methods that provide detailed of ~500 mm total length (TL) and has a detritivorous- information on the movement of individuals, is the herbivorous diet [34]. Collection of large numbers of high incidence of resident individuals within migratory juveniles in the lower reaches of the Daly River, Northern populations, a phenomenon referred to as partial Territory, Australia after the wet season (King, A. unpub migration [19]. Skipped breeding partial migration is one data) and recent otolith chemistry analyses demonstrate type of partial migration when resident individuals forgo migration from saline to fresh water [35] confirming a breeding migration some years. In diadromous fishes, this catadromous life history as reported by [36]. Gonad mat- is the case when mature individuals skip spawning, as uration occurs in fresh water, and stable isotope analysis reported for several species, such as sturgeons (Acipenser suggests that food source do not vary seasonally [37]. P. brevirostrum, [20]), salmonids [21,22] and barramundi ordensis could be considered as semi-catadromous as it (Lates calcarifer, [23]). Skipped spawning is a common is unclear if adults spawn in the estuary or in the ocean strategy in fish [24,25] that provides fish with the ability [34]. P. ordensis is an important prey species for high-order to maximize their adult individual fitness in response to predators in Northern Australian rivers, including teleost 42   Saboret et al. fishes (e.g.,barramundi Lates calcarifer, forktail catfishes transversely sectioned to a thickness of 300 mm through Neoarius spp.), euryhaline elasmobranchs (bull shark the primordium using a low-speed saw. The sections were Carcharhinus leucas, northern river shark Glyphis garricki), polished using lapping film (9 mm), rinsed with deion- the estuarine crocodile Crocodylus porosus [38] and ised water, air dried and mounted on glass slides using piscivorous birds (e.g. white bellied sea eagle Haliaeetus epoxy resin. We used fish otoliths to infer fish growth, age leucogaster, eastern great egret Ardea modesta, Whistling and length at freshwater entry, and spawning migratory Kites Haliastur sphenurus) [39]. Given its catadromous life pattern (see below). history and its importance in food webs, P. ordensis likely acts as an important cross-boundary subsidy, sustaining predators in rivers [40]. 2.2.2 Otolith ageing for fish growth and mortality The study was conducted in the Daly River (DR) and estimation South Alligator River (SAR), Northern Territory, Australia. The region is a tropical savannah characterized by a mon- For otolith ageing, annual growth increments were identi- soonal climate with distinct wet and dry seasons. Rainfall fied according to previous studies on other mullet species is extremely seasonal, with 95% falling in the wet season [46,47] and measured along the otolith chemistry tran- between October and May (Australian Bureau of Meteor- sect under 100X magnification using a stereomicroscope ology), driving high river flow and vast highly productive and image analysis software (Image-ProPlus, ver 4.2, floodplains [41]. The main channels are considered olig- Media Cybernetics, Rockville, MD, USA). The relationship otrophic and heterotrophic [42]. between age and SL was analysed using the von Bertalanffy $%∗(($)) equation of the type SL (t) = SL . )1− e - !"# where SL is the maximum SL of the fish, K is the max 2.2 Fish growth and migratory pattern from growth coefficient, l is the time reference and t is the fish age [48]. The model was fit using the function nls in R otoliths (Additional material: Fig. S1, R² = 0.71) and we found l = 2.2.1 Otolith collection and preparation 0.32, K = 0.332 and SL = 500.1 mm. We used a function max of the type 𝑊𝑊 = 𝑎𝑎 ∗𝐿𝐿 [49] to examine the relationship For otolith ageing and microchemistry, individuals were between SL and body mass of aged fish, where W is the collected and euthanized from the DR, in the late dry weight, L is the standard length, a and b are species-spe- season/early wet season (Jul.-Oct) 2012- 2013 (n=47; 88-395 cific parameters. We did not find differences in residuals mm standard length (SL), 18.1-1768 g) and wet season (Jan.) between sexes (one-way ANOVA including males, females 2014, from the SAR (n=25; 240-380 mm SL, 244-1358 g) and juveniles, F = 0.79, P = 0.46) or sites (one-way ANOVA, (Fig. 1). Fish were sampled by boat electrofishing from the F = 1.9, P = 0.10), suggesting no effect of sex on growth main river channels, far upstream (70-120 km) the estuary trajectory. Data were log-transformed and examined with mouth and thus representing freshwater dwellers. Upon least squared regression (Additional material: Fig. S2, R² capture, fish were immediately euthanized by overdose in = 0.99). Combining the two models, weight-at-age was Aqui-S (175 mg L-1242) and measured and weighed to the described by: nearest mm and g, respectively. The sagittal otoliths were !"∗(%!&) ( (1) W(t)= a .*1− e - removed in the field and placed into labelled paper enve- lopes for storage prior to preparation for analysis. Otoliths are calcified structure of the inner ear of fish, made of suc- cessive layers of calcium carbonate and proteins that act 2.2.3 Migratory patterns based on otolith as a record of growth and environmental conditions expe- microchemistry rienced by fish [43]. Otoliths are characterized by annual increments due to seasonal variation in metabolism which A multi-collector laser ablation-ICP-MS was used to provide the ability to age fish and back-calculate growth 87 86 measure Sr isotope ratios ( Sr/ Sr) from the core to edge [44]. As the otolith grows, its composition also reflects of transversely sectioned sagittal otoliths following the the environmental water chemistry. In particular, ratios methods outlined in [35,50]. Four fish were removed from 87 86 of strontium isotopes ( Sr/ Sr) are indicative of experi- the analysis because examination showed that the laser enced water salinity [35,45]. In preparation for analysis, transect did not traverse the primordium due to sample one sagittal otolith from each fish was embedded in two- preparation issues. An algorithm was used to consistently part epoxy resin (EpoFix; Struers, Ballerup, Denmark) and Partial migration drives subsidy allocation  43 determine the timing of freshwater entry based on the to ensure that the model was biologically relevant [52]. We 87 86 Sr/ Sr transect data for each fish following three criteria: used those relationships to back-calculate the length and 87 86 (i) Sr/ Sr ratio above 0.7096, corresponding to a salinity weight of fish at freshwater entry. We identified migration !" of <5 g.L in both rivers [23,35]; (ii) a local increase of to brackish water by visually identifying portions of the 87 86 87 86 Sr/ Sr ratio corresponding to a migration into less saline Sr/ Sr transects that were below or close to the value of 87 86 water; (iii) and an increase in the Sr/ Sr ratio (>2‰ / 50 0.7096 (Fig. 2). This value corresponds to a salinity of at -1 µm of transect) indicating sustained fresh water residence least 5 g.L during the wet season, according to previous (Fig. 2). We examined the relationship between otolith sampling and mixing models in the DR [35], and the SAR 87 86 core-to-edge transect distance and fish SL (mm) and [23]. In both rivers, Sr/ Sr show little change above 2 -1 87 86 weight (g) with least squared regression, assuming linear g.L , and a sharp decrease in otolith Sr/ Sr is indicative and log-linear relationship, respectively, in this range of a transition to brackish waters. of size (Additional material: Fig.S3, R² = 0.76) [51]. The analysis included a broad range of fish size (88-375 mm SL) A B Timor sea South Alligator River Daly River Gulf of NORTHERN Carpentaria TERRITORIES Australia C E D F Figure 1: (A) Map of the study area. (B) Zoom in the South Alligator River, orange circles show acoustic antenna locations, down to the estuary. (C) Aerial photography of the South Alligator River. (D) Photography of Planiliza ordensis, (E) shows the surgical implantation of an acoustic transmitter. (F) Example of a core-to-edge otolith transect. Diamonds show the location of annual rings. 44  Saboret et al. 2.3 Individual survival based on population ble and averaged 77 m (±48 SD) in length (range = 5–263 m). At the completion of each electrofishing shot, fish survey were counted and measured (SL) to the nearest mm, and As part of another study, 929 P. ordensis were surveyed returned alive to the point of capture. biannually in both the early and late dry season, over a We used length data to ensure that the back-calcu- 7-year period from 2006–2012 in the DR catchment. A lated size at freshwater entry determined by otolith micro- complete description can be found in Keller et al. 2019. chemistry was consistent with field data. We also used In brief, fish were sampled at discrete multiple locations those data to infer mortality in fresh water. As length did (shots or replicates) using a boat or backpack electrofish- not significantly differ between years (see Results), this ing (pulsed DC), depending on water depth. Electrofisher effect was not further considered. We used the von Ber- settings were adjusted to maximise efficiency of collect- talanffy equation that we established with otolith ageing ing fish with minimum power. At least 15 electrofishing (see above) as an age-length key to transform fish length shots of five minute elapsed duration were undertaken for to age and estimate population age structure [55]. As the each sampling event, and shots were stratified to ensure size structure did not differ between early and late dry each available habitat type within each site was sampled season (see Results), we pooled all age data by normaliz- at least once. Prior examination of sampling efficiency ing age structure to early dry season. We assumed that fish has revealed that 15 shots yields an accurate estimate of under 2 years were under-estimated due to sampling bias; species composition and assemblage structure within thus, we calculated disappearance for fish >2 years as the each site (Kennard et al. unpubl. data). Electrofishing proportion of fish missing between an age class and the shots were conducted in as homogenous area as possi- subsequent one. A B C D E F Core-to-edge distance (µm) Figure 2: Example of core-to-edge transect of otolith 87Sr/86Sr in individual P. ordensis from the Daly River (A-D) and South Alligator River (E-F). Blue dotted lines show the marine value of 87Sr/86Sr. Black diamonds show the location of annual increments. Green triangles show the predicted location of freshwater entry (see Methods). The two stars show example of seaward spawning migrations. 87 86 Srൗ Sr Partial migration drives subsidy allocation  45 2.4 Adult spawning behaviour and mortality test, we checked normality of data (Shapiro-Wilk tests and Q-Q plots). from acoustic tracking Data from 25 P. ordensis that were tracked in the SAR using acoustic telemetry were used to directly monitor 2.6 Allocation of subsidy modelling movements of fish into the putative spawning grounds and derive a second, independent mortality rate estimate We modelled the mean net biomass flux to freshwater that for comparison with the estimate from population age was driven by an individual P. ordensis, using an individ- structure [56]. Fish were collected by boat electrofishing ual mass balance approach, considering biomass that was and tagged by surgically implanting acoustic transmit- acquired in one biome and delivered to the other biome. ters (Vemco V13, 36 mm length, 11 g, 695 days estimated Given that diamond mullet mature in freshwater [37] and battery life, Vemco, Nova Scotia). Fish were adults, that movement in the marine environment is limited (see between 300-370 mm standard length (SL), mean 336 (±21 Results), we considered that most of biomass was delivered SD) mm SL. A complete description of the tagging method in the form of prey. Therefore, we only considered subsidy is provided by [23]. in the form of fish biomass as prey or carcasses for scav- An array of 30 acoustic receivers was deployed from engers (i.e. did not consider excretions), and considered the freshwater reaches of the SAR to the estuary mouth that fish disappearance was indicative of predation given (Fig. 1). As detections of all fish were contained within the high abundance of predators and scavengers in the the region covered by the acoustic receiver array, disap- system. The model only considered the delivery of alloch- pearance of telemetered fish within the battery life of the thonous biomass, therefore not considering juveniles transmitters was assumed to reflect mortality [57]. The that never migrated to fresh water and freshwater-derived sudden cessation of detection is a strong indicator of mor- biomass of fish that died in the river, which corresponds tality [58], as the only alternative hypothesis would be tag to organic matter turnover. We assumed negligible effects expulsion (which usually occurs shortly after tagging [59]) of growing during spawning residence in the marine envi- or tag malfunctioning (which is not expected [60]). ronment, meaning that marine-derived biomass was only We calculated the mortality rate using a full year of acquired before freshwater entry. We defined the freshwa- th th acoustic data from October 20 2013 to October 20 2014. ter-marine ecotone as the limit between inland water and Survival was computed using the function survfit in the the estuary. package survival [61], using the tsiatis method to estimate Thereby, net subsidy into fresh water (S) was calcu- survival error [62]. Ten of the 25 tagged mullet were not lated as the difference between the flux of marine-de- detected during the study, suggesting mortality in the rived biomass of fish dying in freshwater (Φf) and the immediate post-tagging period; possibly due to the relative flux of freshwater-derived biomass of spawners dying sensitivity of the species to handling and the harsh envi- in seawater (Φs): ronmental conditions at the time of collection and tagging -1 (water temperature >34°C, dissolved oxygen <1 mgL ). The (2) S =Φf– Φs, remaining 15 fish exhibited wide-ranging movements and we assume there were no long-term tagging effects for With Φf corresponding to the mass at freshwater entry these fish [63]. One fish was last detected at the furthest (𝑊𝑊 ) that is effecti vely delivered to fresh water by !"#$%& upstream antenna, and thus we could not determine its fish that die in freshwater, and can be defined as a fate and we did not include it in the survival analysis. gross subsidy into freshwater: 0* (3) 𝛷𝛷𝛷𝛷 = $ 𝑃𝑃 (𝑡𝑡 ) .𝑃𝑃 (𝑡𝑡 ) .(1− 𝑃𝑃 (𝑡𝑡 ) ).𝑊𝑊 𝑑𝑑𝑡𝑡 !"#$% #'()" *(+,#$(-+ ."-$,/ 0."-$,/ 2.5 Statistical analysis And Φs corresponding to the mass derived from freshwa- All data analysis, statistics and modelling were done in R ter that is effectively delivered to seawater by spawners version 4.0.2 [64]. that do not return from spawning: To test for effect of sex on skipped spawning rates, 0* 𝛷𝛷𝛷𝛷 = $ 𝑃𝑃 (𝑡𝑡 ) .𝑃𝑃 (𝑡𝑡 ) .𝑃𝑃 (𝑡𝑡 ) .(𝑊𝑊 (𝑡𝑡 )−𝑊𝑊 ) 𝑑𝑑𝑡𝑡 effect of sex and size on weight-to-length relationship (4) !"#$% #'()" *(+,#$(-+ ."-$,/ residuals, and effect of seasons and years on age fre- quency, we performed one-way ANOVA tests. For each 46  Saboret et al. 3 Results 𝑃𝑃 (𝑡𝑡 ) 𝑃𝑃 (𝑡𝑡 ) 𝑃𝑃 (𝑡𝑡 ) 𝑊𝑊 (𝑡𝑡 ) !"#$% !"#$% !"#$%&"'# , , and are the probability of dying, being alive, migrating (i.e. being in seawater), and weight at age t, respectively. Tfentry, Tf and 3.1 Migratory patterns of P. ordensis Tm are the age at freshwater entry, first and last spawning 𝑊𝑊 !"#$%& migration, respectively. is the weight at freshwa- Estimated fish ages ranged from 1 to 6 years, with a ter entry, which corresponds to the biomass derived from mean of 2.9 years (SD=0.9). In the DR, the seasonal 87 86 seawater.. oscillations in Sr/ Sr ratio between 0.72 and 0.73 We assumed that mortality was independent of time (characteristic of the main channel, see [35]) matched 87 86 of the year, age and habitat (see Results). Therefore, S was with annual increments and Sr/ Sr in between the pri- simply calculated as: mordium and the first increment were very close to the marine value of 0.70907 [67], confirming marine resi- (5) dence in the juvenile phase and catadromy (e.g. Fig. 2). Of the 68 fish examined, 66 (97%) showed a clear tran- 87 86 𝑃𝑃 Where ss is the skipped spawning rate, is the sition in otolith Sr/ Sr from marine to fresh water (Fig. !"#$% annual mortality and Δt the time spent in the estuary. 2). The two fish which did not exhibit such a transition The equation corresponds simply to the marine-derived were small fish (<125 mm SL) and had likely migrated biomass that is imported into fresh water by migrating into fresh water just prior to capture, leaving insuffi- 𝑊𝑊 (𝑡𝑡 ) juveniles ( ) subtracted by the biomass that cient time for incorporation of the freshwater chemical 𝑊𝑊 !"#$%& is exported by spawners (1−𝑠𝑠𝑠𝑠 ) that are still alive at signature (see [68]); in these cases the core-to-edge dis- $'( 𝑃𝑃 time t ((1−𝑃𝑃 ) ) and die in the estuary ( Δt ), tance was taken as freshwater entry. Age at freshwater !"#$% !"#$% throughout life of adult fish (integral from Tf to Tm). The entry ranged between 0+ year (44% of individuals) and equation was computed numerically using a daily incre- 1+ year (56%). Back-calculated SL at freshwater entry ment. Table 1 summarizes how the different parameters was normally distributed (Shapiro-Wilk test, W-statis- have been inferred. tic=0.98, P=0.39), with a mean of 147 mm (SD=26) (Fig. 3A). This corresponded to an individual mass of an average 72.8g ([62.8, 82.8] 95% CI). Length-frequency 2.7 Model extension to other diadromous data were consistent with the estimated size at fresh- water entry from otolith back-calculation, with only fishes two fish <90 mm SL recorded from freshwater (Fig. 3C). The model was used to investigate how migratory behav- Otolith chemistry revealed few migrations into the iour (age at first migration and skipped spawning) of other marine environment (14 % of fish between 2 and 3 years diadromous fishes might affect nutrient fluxes, in relation N=43, 0% of fish beyond 3 years N=9; Fig. 2A, C). The to annual mortality and growth coefficient, two parame- acoustic telemetry showed that five of the 10 fish still ters which are subject to broad variations among systems being tracked after the late wet season had migrated due to external influences [65,66]. The model extension downstream into the putative spawning grounds down- is based on the premise that diadromous fishes use one stream the lower estuary (Fig. 4A). Residence times of biome for growth, and the other biome to spawn and some migrating fish in the lower estuary were very short grow as early juveniles, therefore excluding feeding in the (only a few days), which may explain the lower number of spawning biome and omitting excretions in the spawning migrations detected by otolith chemistry analysis: short- biome for simplification. For the purposes of this explor- term migrations can be difficult to detect using otolith atory modelling exercise, key life history traits were held chemistry due to the laser spot size and time taken for at the same value (maximal age fixed at 10 years; maximal otolith chemistry to reach equilibrium with the ambient weight fixed at 10 kg; same growth model (equation (1)); water [68]. Nonetheless, both the otolith chemistry and constant mortality) so that predicted subsidy differences acoustic tracking data suggested a high proportion of only reflect migration behaviour differences. skipped spawning each year. Altogether, our data showed a high skipped-spawning rate (~50% and 85% from telem- etry and otolith chemistry, respectively) and for the pur- poses of modelling, we used an annual skipped spawning rate of 50% for P. ordensis (Table 1). We also assumed that fish spent an average of 4 months in the estuary based on Partial migration drives subsidy allocation 47 our telemetry and otolith data, and previous studies [34] beyond 2 years [35], supporting that disappearance was (Table 1). Although sample size was low (n=35), the otolith reflective of mortality. chemistry data suggested no bias in skipped spawn- Tagged fish were detected frequently by the passive ing rates among sexes for mature individuals (one-way acoustic receiver array, with average delays between ANOVA, F = 0.09, P = 0.76). detections of 2.5 hours and the maximum time between detections averaging 41 days (min = 1 d, max = 110 d). This frequency of tag detection, the lack of detections on 3.2 Mortality of P. ordensis the most downstream loggers in the system for most fish, and the estimated tag battery life of ~2 years, all support Age frequency data for the DR did not differ between years our assumption that fish that were undetected for >1 year (one-way ANOVA, F = 1.84, P = 0.2) and seasons (Fig. 3C, had suffered mortality within the system. The acoustic one-way ANOVA, F = 0.63, P = 0.46), and thus was mod- tracking showed a relatively constant rate of decrease elled as an age-independent disappearance rate of ~60% in the number of tagged individuals detected through- 87 86 for fish > 2 years of age (Fig. 3D). Otolith Sr/ Sr ratio sig- out the year (Fig. 4B), suggesting that time of the year natures in the same system suggested that no emigration (i.e., seasons) did not strongly affect the mortality rate. from another system (such as tributaries) occurred for fish Although the number of individuals was low, estimates of annual mortality from the acoustic telemetry were high A B Figure 3: (A) Distribution of back-calculated length at freshwater entry of P. ordensis. Blue line shows the normal distribution of the data. (B) Distribution of back-calculated weight at freshwater entry of P. ordensis. Blue line shows the normal distribution of the data. (C) Length distribution of P. ordensis from the Daly River, obtained by biannual sampling in 2012 (King A., unpub. data.). Blue line shows the mean back-calculated length at freshwater entry. (D) Age structure of P. ordensis >2 years. Open circles show the calculated disappearance rate between age classes. Bars show 95% confidence interval of disappearance rate. 48   Saboret et al. the low proportion of migrating individuals (i.e. skipped spawning). Skipped spawning was a strong factor affect- ing subsidy allocation. For an annual skipped spawning rate of 50% -which appears realistic in this population, see above-, we estimated that each mullet represented a net 42.8g flux into fresh water (Fig. 5). However, absence of skipped spawning would result in near-null balance of fluxes with almost as much biomass exported as imported in freshwater (net flux to fresh water of just 12g). 3.4 Predictions for other diadromous fishes Extending the model to other life-history traits showed that catadromous fishes could allocate a net biomass flux to either marine or freshwater habitat (Fig. 6). Skipped spawning rate was an important driver of the allocation. Populations with low skipped-spawning rate (i.e. most of individuals migrate every year) could only represent a net flux into fresh water under high mortality that prevented most of individuals from growing to large size and export- ing biomass when migrating to spawn. In populations with high skipped-spawning rates, the export of biomass remained limited, generally resulting in a net subsidy for Figure 4: Acoustic telemetry tracking of 15 P. ordensis over one freshwater ecosystems. In that case, the magnitude of the year in the South Alligator River. (A) Survival estimate against time. subsidy depended mostly on the mass at freshwater entry, Dashed line denotes 95% confidence estimate. (B) Location of detection events, each colour showing one individual. Stars (on the which was determined by growth and age at freshwater right) show the locations of acoustic antennas. Crosses show esti- entry, while mortality had limited influence because most mated fish death (loss of record, see Methods). Question mark “?” of individuals died while in freshwater. denotes uncertain fate of the fish (death or upstream migration). Given that catadromous and anadromous fishes are broadly symmetrical, the direction of the biomass flux at around 80% ([0.45, 0.96] 95% CI) which overlapped was inverted in the case of anadromous fish. Populations with the estimate from age structure. Altogether, our data of anadromous fish with high skipped-spawning rates suggest a relatively constant, age- and habitat-independ- could only act as a net import of biomass to fresh water ent mortality rate of approximatively 60-80% per year if juveniles migrate early to the seawater, growth fast in (Table 1). the marine environment and there is high survival (Fig. 6). 3.3 Allocation of subsidies 4 Discussion The maximum subsidy per individual to fresh water cor- responded to the mass at fresh water entry ~72 g that was 4.1 Prevalence of skipped spawning estimated from otolith back-calculation and supported by population survey data (Fig. 5). Before the first spawning There is growing evidence that migration is a highly migration, 80% of this flux was effectively delivered to variable phenomenon at the individual level [69], and freshwater food webs due to high mortality, corresponding Thomson noted many decades ago that populations of a to gross flux to fresh water. Despite the fact that mature catadromous mullet, Mugil cephalus, were composed of individuals weigh much more that juveniles at fresh water individuals forgoing seaward spawning migration [70]. entry, the flux from fresh water to seawater was damp- Otolith microchemistry further confirmed high prevalence ened by the low survival, the relatively high probability of skipped spawning in M.cephalus with some individuals for adults to return to fresh water (i.e. iteroparity) and staying in fresh water for extended periods (>7 years) [71]. Relative survival Partial migration drives subsidy allocation 49 Table 1: Parameter estimates used to model nutrient fluxes in the study. Parameter Estimate Parameter (Equation) Method Length-weight relationship log(a)=-11.0, b=3.05 a, b (1) Fish collection Size parameter 0.32 l (1) Otolith ageing Growth rate 0.332 K (1) Otolith ageing Maximum length 500.1 mm SL (1) Otolith ageing max Weight at freshwater entry 72.8g W (5) Otolith microchemistry, fish survey fentry Age at first spawning 2 years T (5) Otolith microchemistry, acoustic telemetry Maximum age 7 years T (5) Fish survey -1 Mortality rate 0.6. year P(t) (5) Fish survey, Acoustic telemetry death Time in the estuary 4 months Δt (5) Acoustic telemetry Skipped spawning rate ~50% ss (5) Otolith microchemistry, Acoustic telemetry A B Seawater Fresh water Cumulative net flux in fresh water (g/individual) Migrant ɸf Juvenile Freshwater ~1 year entry Larva Maturity >2 years Eggs migration Weight x8 Skipped Survival 21% spawning Fish age (years) ɸf-ɸs migration Skipped spawning ɸs Weight x28 Survival 0,6% Skipped 0% 50% Spawning: Figure 5: (A) Life history of P. ordensis, as inferred from otolith microchemistry, age-at-length data and acoustic telemetry. Φf (Flux into fresh water, blue arrow) and Φs (Flux into seawater, green arrows) represent the flux of biomass across the freshwater-marine ecotone, as calculated in equation (3) and (4). (B) Dashed line: relative survival after freshwater entry, dotted line: relative weight, continuous line: net cumulative flux in fresh water. After freshwater entry, migrating juveniles start to be preyed in the river resulting in a positive net cumulative flux from the marine to the freshwater environment. Before the first spawning migration, around 80% of mullets have been preyed, meaning that 80% of the mass at freshwater entry (73 g) has been delivered to the river food web. After maturation, the flux is inverted as individuals start to migrate and some do not return from seawater. Older individuals contribute relatively less to fluxes as the increase in biomass is out- weighed by the decrease in survival, given our parameters. With increasing proportion of individuals migrating (skipped spawning from 0% to 50%), fluxes to seawater proportionally increase. The net flux of subsidies into fresh water is the cumulative net flux at final age, which is the sum of a continuous incoming flux after freshwater entry -as all individuals derive some mass from their marine phase- and outgoing fluxes at spawning migration –driven by much fewer individuals of bigger mass. Age at first migration 1,2 0,8 1 50   Saboret et al. Skipped spawning Average subsidy 20% 50% 80% per individual (%/total mass) 0.55 into fresh water 0.45 0.35 0.25 0.55 0.45 0.35 0.25 0.55 -5 0.45 0.35 -10 0.25 0.2 0.4 0.6 0.8 0.2 0.4 0.6 0.8 0.2 0.4 0.6 0.8 -15 Mortality Mortality Mortality Figure 6: Modelling of the allocation of subsidies across the freshwater-marine ecotone driven by an iteroparous catadromous fish, accor- ding to intra-variation life history (see Methods). Skipped spawning increases from the left to the right and age at first migration from the top to the bottom. For a given skipped spawning and age at first migration (i.e. within an individual square), mortality increases from the left to the right and growth from the bottom to the top. Shade of colour shows the direction and magnitude of subsidy in fresh water (kg) for a hypothetic fish that could reach 10 kg at a maximum age of 10 years (see legends). Given that catadromous and anadromous fishes play sym- metrical roles, the direction of the biomass flux is simply inverted in the case of an iteroparous anadromous fish. In line with these studies, our study of P. ordensis showed tion of post-spawned individuals by otolith microchemis- that only a subset of mature individuals migrated every try (i.e. some fish survived spawning migration). In both year to the spawning grounds. Skipped spawning can be cases, telemetry suggested that most fish are preyed upon explained by a trade-off between the benefit and cost of in fresh water before they reach the estuarine spawning spawning over the long term, as individuals can maxi- grounds. mize their cumulative reproductive output by skipping breeding, reducing mortality risk and devoting resources towards growth [24,25]. P. ordensis is a capital breeder (i.e. 4.2 Net import of biomass driven by P. store energy for latter reproduction [72]) which accumu- ordensis lates fat during the wet season in productive floodplains and allocates this energy for reproduction during the To our knowledge, this study is the first estimate of the dry season [37]. In the case of migratory fishes, skipped direction of biomass fluxes driven by a catadromous fish spawning might be especially common because of the across the freshwater-marine ecotone. Using an individual mortality risk and energetic costs associated with migra- mass-balance approach, we showed that skipped spawn- tion [26]. In our study, we could not clearly conclude from ing dampened the flux of biomass to the sea, resulting in a telemetry if mortality was higher for migrants because net subsidy of on average ~43 g to freshwater ecosystems. some individuals could move downstream without the This magnitude of subsidy is likely to be important at the intention of breeding. The estimated annual mortality rate ecosystem level as P. ordensis is a common prey species of ~60% and the observation of high mortality outside the for high-order predators in Northern Australian Rivers migration period suggest that either very few individuals [33,38], and given observations of massive schools of migrate at high mortality cost, or that the mortality cost mullet entering fresh water (authors pers obs.). The alloca- of migration is low, which is supported by the observa- tion of prey to one or another habitat can have bottom-up Growth Growth Growth Partial migration drives subsidy allocation  51 effects on predators [30], with far-reaching consequences requirements of this species to migrate from freshwater to on ecosystem functioning [73]. This input of marine-de- marine spawning grounds, one might predict that barra- rived biomass could carry essential nutrients and energy mundi acts as a net export of energy to the sea. However, to sustain high productivity in those ecosystems while this species also shows a high variability of migratory being limited in nutrients most of the year [42]. Even small strategies [81], including a high prevalence of skipped subsidies can play a critical role in ecosystem processes. spawning [23], which our model suggest may invert the For instance, the migration of mayflies can increase juve- source-sink coupling between marine and freshwater eco- nile salmon growth in a one-to-three ratio and sustain in systems. cool tributaries populations of fish that are key ecosystem We expect that the predictions of our models may engineers [74]. apply to other diadromous fishes. However, it is worth Although our study only considers the net direction noting that our model only considers subsidies in the form of fluxes to identify source and sink across the freshwater- of fish biomass and might not apply to specificities of other marine ecotone, it should be recognised that the potential life histories [82]. Some fish, such as Atlantic salmons, effect of subsidies also relies on the quality of energy consume most of their energy reserves (up to 70%) for long [75] and delivery pathways within food-webs [76,77]. For distance migration, maturation and sexual development instance, marine subsidies can be critical for freshwater [83]. By doing so, fish contribute subsidies in the form of ecosystems because of their role in supplying high quality excreted nutrients in the spawning habitat. For instance, fatty acids [78] or micronutrients [79], rather than simple anadromous shad lose ~30% of weight while migrating mass-balance processes. Our study also only focused on from the marine environment into rivers [84]. However, the fluxes between seawater and fresh water, but it is nutrients that are excreted in the growing habitat (e.g., worth noting that P. ordensis also contribute to moving energy reserve consumed by salmons in the ocean) do not energy within those biomes. Despite the fact that juvenile contribute to biomass flux across the freshwater-marine growth appears to occur in seawater, adults might spawn ecotone as they represent turnover of autochthonous (i.e. and be preyed in the intertidal zone. Within the river, formed where it is found) organic matter. growth could be supported by terrestrial carbon [40] While our model contains several simplifications, and be allocated in other reaches of the streams [54], or we believe it has potential utility as a framework in many even return to terrestrial ecosystems via predation by cases to examine the allocation of biomass by diadromous birds. Therefore, although the study focused on fluxes fishes. For example, iteropareous Atlantic salmon (Salmo across the freshwater-marine ecotone, it is worth noting salar) are usually considered as transporters of energy that diadromous fish like P. ordensis may also transport and nutrients to streams [85,86]. However, they also show biomass within and into other biomes. high variability in reproductive strategy [87], with some populations composed of only ~5% repetitive spawners [88]. Thus, despite the high ratio of adult:juvenile mass, 4.3 Revisiting the role of diadromous fishes we suspect that iteroparous anadromous salmonids, such as Atlantic salmon, could in some instances act as on the allocation of subsidies across the an export of energy to the sea in populations where when freshwater-marine ecotone skipped spawning is common. This prediction is in line Contrary to expectations [18], our model predicted that with historical estimates showing that even semelparous fresh water may act as a sink of marine-derived biomass Pacific salmon (Oncorhynchus spp.) could act as a net flux driven by a catadromous fish. Given the very high abun- of nutrients to the sea when the proportion of returners is dance of P. ordensis and other catadromous species, such low [89]. as barramundi, Lates calcarifer, tarpon, Megalops cypri- This inversion of nutrient flux was also explained by noides, and other mugilids across northern Australia, we a nonlinear relationship between spawner abundance extended our model to other life-history traits. The exten- and the number of migrating smolts [90], illustrating sion of the model shows that when considering skipped that density dependence processes may drive feed-backs spawning, catadromous fishes are much more likely to act between fish life-history (e.g. the proportion of spawners) as a net biomass flux to fresh water. For instance, barra- and biomass fluxes. In addition, while the direction of mundi are characterized by relatively rapid growth [80], subsidies is determined by individual life history, the mag- high ratio (>10) between mass at spawning and at fresh- nitude also depends on population dynamics. Increased water entry, and relatively higher survival than P. orden- skipped spawning by P. ordensis results in retention of sis based on telemetry and ageing [23]. Considering the biomass in fresh water, but could also decrease the total 52   Saboret et al. amount of subsidies over the long term, as fewer indi- Kakadu National Park research permits RK786, RK805 and viduals spawn, resulting in lower biomass flux of juve- RK862. niles. In turn, skipped spawning is a conditional strategy in fish [22,24] that is strongly affected by environmental conditions. More studies are needed to integrate the rela- Acknowledgements tionship between the import and export of biomass in dynamic systems, and the implications for subsidy stabil- We gratefully acknowledge traditional indigenous owners ity with regards to environmental variation. of those parts of the South Alligator River (the Bininj and Mungguy people) and the Daly River (the Wardaman, Jawoyn, Wagiman and Malak Malak people) in which this study took place, and thank them for providing access 5 Conclusion to their land. Anne O’Dea (Parks Australia) coordinated Indigenous consultation within Kakadu National Park The model derived in this study offers a simple tool to and provided assistance with logistics and field activities. examine subsidy allocation across the freshwater-ma- Staff from the Department of Industry, Tourism and rine ecotone by diadromous fishes. We show that skipped Trade (NT Fisheries), in particular Quentin Allsop and spawning in a catadromous fish can lead to a net import Wayne Baldwin, are thanked for assistance with the of subsidies in freshwater ecosystems. Furthermore, we collection of fish. Peter Kyne led the set-up, maintenance highlight that variation in migratory behaviour in other and downloading of the acoustic telemetry array. We diadromous fishes could affect the source-sink coupling gratefully acknowledge John Woodhead, Roland Maas between the ocean and inland waters. Fish migration and Alan Greig (University of Melbourne) for assistance behaviours are affected by recent human disturbances, with the otolith chemistry analysis. Fish samples were such as artificial barriers [91], global warming [92] and obtained from the Daly River Fish Monitoring Project, with fishing pressure [93]. The tropical river systems of Austral- financial support from Charles Darwin University and the ia’s north are not exempt from environmental threats and Northern Territory Government. Funding for this research our study highlights that conservation effort should be was provided by the Australian Government’s National directed towards protecting connectivity between rivers Environmental Research Program. GS was supported by an and the sea to preserve the integrity of energetic fluxes international internship from Ecole Normale Supérieure across ecotone boundaries. de Lyon, France. Author contribution References DC, MD and AK designed the study. DC, DB, AK and MD [1] Loreau M, Holt RD. Spatial Flows and the Regulation of collected the data. GS and DC analysed the data. GS led Ecosystems. Am Nat. 2004;163:606–15. the writing of the manuscript with substantial input from [2] Polis GA, Wendy B. Anderson1, and, Holt RD. TOWARD AN DC. 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The impact of fishing-induced mortality on the evolution of alternative life-history tactics in brook charr. Evol Appl. 2008;1:409–23. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Animal Migration de Gruyter

Partial migration in diadromous fishes drives the allocation of subsidies across the freshwater-marine ecotone

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Anim. Migr. 2021; 8:40–55 Research Article Grégoire Saboret, Duncan J. Buckle, Alison J. King, Michael M. Douglas, David A. Crook Partial migration in diadromous fishes drives the allocation of subsidies across the freshwater- marine ecotone https://doi.org/10.1515/ami-2020-0108 P. ordensis acted as a net 42.6g biomass subsidy in fresh received April 30, 2021; accepted August 17, 2021 water, representing a retention of more than 50% of the juvenile mass at freshwater entry. Our model predicts Abstract: Migratory animals can act as cross-boundary that skipped spawning is likely to alter the allocation of subsidies sustaining ecosystem functioning, such as subsidies in diadromous species, highlighting the impor- diadromous fishes that migrate between fresh water and tant effects of individual variation in migratory behaviour seawater and carry nutrients and energy across the fresh- on fluxes of energy and nutrient at ecosystem scales. We water-marine ecotone. Frequency and timing of migration encourage future studies to consider how variation in are however highly variable within and among popula- migratory behaviour is likely to affect the direction and tions. We hypothesized that in catadromous fishes (i.e., magnitude of biomass fluxes across ecotone boundaries. diadromous fishes that grow in freshwater and spawn in Keywords: Partial migration; Skipped spawning; Cata- the sea, such as eels), the import of subsidies by migra- dromy; Marine-derived nutrients; Prey availability tory juveniles could outweigh the export of subsidies by adults due to skipped spawning migration. We used the diamond mullet Planiliza ordensis, as a model species, and determined life-history traits using a combination of length-to-age data, acoustic telemetry and otolith (fish ear stone) microchemistry. We used a mass balance approach 1 Introduction to model individual mass acquisition and allocation, and extended our model to other life-history strategies. Our Most ecosystems are recipients of allochthonous resources results showed high intra-population variation of migra- (i.e. not originating in the region where they are found), tory behaviour in P. ordensis, with few individuals migrat- such as nutrient, organic matter and prey, that enhance ing every year to spawn. We estimated that an individual in situ productivity [1,2]. Recent theoretical and empirical studies suggest that low to moderate allochthonous inputs (or ‘subsidies’) can stabilize trophic dynamics, defined as the movement of carbon, nutrients, and energy among organisms in an ecosystem [3,4]. However, depending on *Corresponding author: Grégoire Saboret, Research Institute for the the trophic levels that use the resource, trophic dynamics Environment and Livelihoods, Charles Darwin University, Darwin, can become unstable as inputs increase [5,6]. One striking 0810, NT, Australia example is when excessive inputs of allochthonous Master Biosciences, ENS de Lyon, Département de Biologie, 46 allée d’Italie, 69007 Lyon, France carbon from newly inundated riparian areas during high Department of Surface Waters, EAWAG, Center for Ecology, Evolution river flows create hypoxic conditions that can cause large- and Biogeochemistry, 6047 Kastanienbaum, Switzerland, Email: scale deaths of fish and other riverine organisms, and thus saboretgregoire@gmail.com the loss of the steady state [7,8]. Similarly, the transfer Duncan J. Buckle, Alison J. King, Michael M. Douglas, Michael M. of large amounts of organic matter from agricultural Douglas, David A. Crook, Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, 0810, NT, Australia activity into natural ecosystems can fundamentally alter Alison J. King, David A. Crook, Centre for Freshwater Ecosystems, trophic dynamics: trophic cascades can be initiated and La Trobe University, Albury-Wodonga, 3690, New South Wales, rare or uncommon species can become invasive while Australia functionally important common species decline [9]. Such Michael M. Douglas, School of Biological Sciences, The University of examples demonstrate the sensitivity of ecosystems to Western Australia, 6009, Western Australia, Australia Open Access. © 2021 Grégoire Saboret et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 License. Partial migration drives subsidy allocation  41 variation in the direction, extent and biochemical path- ambient conditions by delaying the timing of reproductive ways associated with subsidies [10]. investment until more suitable conditions occur [26,27]. Migratory animals transport vast amounts of energy It is increasingly recognised that partial migration and nutrients assimilated in body tissues or as waste can affect trophic dynamics in ecosystems [18,28,29]. For products (e.g., faeces, urine) across ecotone boundaries instance, the proportion of migrating cyprinids from lakes [11]. This holds particularly true for diadromous fishes to streams affect the predator community structure [30] and (i.e., fish migrating between seawater and fresh water, may drive the steady state of lakes by a top-down control such as salmons and eels), which connect marine ecosys- on plankton [31]. However, little is known on how partial tems and inland waters via subsidies. One iconic example migration influences the fluxes of energy and nutrients is the migration of Pacific salmons (Oncorhynchus spp.) between the freshwater and marine ecosystems. In the that subsidize streams with marine-derived biomass [12], current study, we hypothesized that skipped spawning which sustain lotic and riparian ecosystem functioning in diadromous fishes could be a main force driving the [13]. There is increasing evidence that other diadromous allocation of subsidies across the marine-freshwater fishes also act as important fluxes of energy and nutrients. ecotone. We used the catadromous diamond mullet, For instance, Engman, Kwak, and Fischer [14] have esti- Planiliza ordensis, an important prey species in riverine mated that the mass migration of tiny diadromous goby food webs of Northern Australia, as a model species. larva (~0.1g each) import a ton of marine-derived biomass We considered subsidies in the form of prey availability, per migration event to a single river because they migrate given the importance of mullets as prey for predators in by millions, representing a significant input of biomass to both environments. Analysis of otoliths (ear bones that the stream. Diadromous fishes include catadromous and act as natural record of growth and migratory pattern), anadromous species that use the freshwater and marine population surveys, and acoustic telemetry were used to ecosystems, respectively, as a growing biome and, marine elucidate individual life-history traits such as timing of and freshwater ecosystems, respectively, as a breeding migration, mortality, growth and migration frequency. We biome [15]. In addition, diadromy also includes amphi- applied our findings to estimate biomass fluxes across the dromy that can be considered as an extension of cata- freshwater-marine ecotone, and then explored our model dromy in which larva drift to the ocean instead of spawner with regards to variation in life-history traits. Specifically, migration [16]. Ontogenetically, diadromous fishes con- we explored how skipped spawning in other diadromous tribute unequally to fluxes: for example, adult Pacific fishes could affect the allocation of biomass between the salmons accumulate most of their mass in the ocean (> freshwater and marine environment. 95%, [12]) and typically weigh one-to-two orders of magni- tude more than out-migrating smolts (e.g 12g vs 5.5kg see [17]). Thus, the direction of spawning migration has been 2 Material and methods proposed as the main driver of nutrient flux, with ana- dromous and catadromous fishes expected to represent a gain and a loss of nutrients and energy for freshwater 2.1 Study species and study system ecosystems, respectively [18]. An emerging theme in research on migratory animals Planiliza ordensis (Family Mugilidae) is endemic to over recent decades, particularly with the advent of Northern Australia [32,33]. It grows to a maximum size telemetry and other methods that provide detailed of ~500 mm total length (TL) and has a detritivorous- information on the movement of individuals, is the herbivorous diet [34]. Collection of large numbers of high incidence of resident individuals within migratory juveniles in the lower reaches of the Daly River, Northern populations, a phenomenon referred to as partial Territory, Australia after the wet season (King, A. unpub migration [19]. Skipped breeding partial migration is one data) and recent otolith chemistry analyses demonstrate type of partial migration when resident individuals forgo migration from saline to fresh water [35] confirming a breeding migration some years. In diadromous fishes, this catadromous life history as reported by [36]. Gonad mat- is the case when mature individuals skip spawning, as uration occurs in fresh water, and stable isotope analysis reported for several species, such as sturgeons (Acipenser suggests that food source do not vary seasonally [37]. P. brevirostrum, [20]), salmonids [21,22] and barramundi ordensis could be considered as semi-catadromous as it (Lates calcarifer, [23]). Skipped spawning is a common is unclear if adults spawn in the estuary or in the ocean strategy in fish [24,25] that provides fish with the ability [34]. P. ordensis is an important prey species for high-order to maximize their adult individual fitness in response to predators in Northern Australian rivers, including teleost 42   Saboret et al. fishes (e.g.,barramundi Lates calcarifer, forktail catfishes transversely sectioned to a thickness of 300 mm through Neoarius spp.), euryhaline elasmobranchs (bull shark the primordium using a low-speed saw. The sections were Carcharhinus leucas, northern river shark Glyphis garricki), polished using lapping film (9 mm), rinsed with deion- the estuarine crocodile Crocodylus porosus [38] and ised water, air dried and mounted on glass slides using piscivorous birds (e.g. white bellied sea eagle Haliaeetus epoxy resin. We used fish otoliths to infer fish growth, age leucogaster, eastern great egret Ardea modesta, Whistling and length at freshwater entry, and spawning migratory Kites Haliastur sphenurus) [39]. Given its catadromous life pattern (see below). history and its importance in food webs, P. ordensis likely acts as an important cross-boundary subsidy, sustaining predators in rivers [40]. 2.2.2 Otolith ageing for fish growth and mortality The study was conducted in the Daly River (DR) and estimation South Alligator River (SAR), Northern Territory, Australia. The region is a tropical savannah characterized by a mon- For otolith ageing, annual growth increments were identi- soonal climate with distinct wet and dry seasons. Rainfall fied according to previous studies on other mullet species is extremely seasonal, with 95% falling in the wet season [46,47] and measured along the otolith chemistry tran- between October and May (Australian Bureau of Meteor- sect under 100X magnification using a stereomicroscope ology), driving high river flow and vast highly productive and image analysis software (Image-ProPlus, ver 4.2, floodplains [41]. The main channels are considered olig- Media Cybernetics, Rockville, MD, USA). The relationship otrophic and heterotrophic [42]. between age and SL was analysed using the von Bertalanffy $%∗(($)) equation of the type SL (t) = SL . )1− e - !"# where SL is the maximum SL of the fish, K is the max 2.2 Fish growth and migratory pattern from growth coefficient, l is the time reference and t is the fish age [48]. The model was fit using the function nls in R otoliths (Additional material: Fig. S1, R² = 0.71) and we found l = 2.2.1 Otolith collection and preparation 0.32, K = 0.332 and SL = 500.1 mm. We used a function max of the type 𝑊𝑊 = 𝑎𝑎 ∗𝐿𝐿 [49] to examine the relationship For otolith ageing and microchemistry, individuals were between SL and body mass of aged fish, where W is the collected and euthanized from the DR, in the late dry weight, L is the standard length, a and b are species-spe- season/early wet season (Jul.-Oct) 2012- 2013 (n=47; 88-395 cific parameters. We did not find differences in residuals mm standard length (SL), 18.1-1768 g) and wet season (Jan.) between sexes (one-way ANOVA including males, females 2014, from the SAR (n=25; 240-380 mm SL, 244-1358 g) and juveniles, F = 0.79, P = 0.46) or sites (one-way ANOVA, (Fig. 1). Fish were sampled by boat electrofishing from the F = 1.9, P = 0.10), suggesting no effect of sex on growth main river channels, far upstream (70-120 km) the estuary trajectory. Data were log-transformed and examined with mouth and thus representing freshwater dwellers. Upon least squared regression (Additional material: Fig. S2, R² capture, fish were immediately euthanized by overdose in = 0.99). Combining the two models, weight-at-age was Aqui-S (175 mg L-1242) and measured and weighed to the described by: nearest mm and g, respectively. The sagittal otoliths were !"∗(%!&) ( (1) W(t)= a .*1− e - removed in the field and placed into labelled paper enve- lopes for storage prior to preparation for analysis. Otoliths are calcified structure of the inner ear of fish, made of suc- cessive layers of calcium carbonate and proteins that act 2.2.3 Migratory patterns based on otolith as a record of growth and environmental conditions expe- microchemistry rienced by fish [43]. Otoliths are characterized by annual increments due to seasonal variation in metabolism which A multi-collector laser ablation-ICP-MS was used to provide the ability to age fish and back-calculate growth 87 86 measure Sr isotope ratios ( Sr/ Sr) from the core to edge [44]. As the otolith grows, its composition also reflects of transversely sectioned sagittal otoliths following the the environmental water chemistry. In particular, ratios methods outlined in [35,50]. Four fish were removed from 87 86 of strontium isotopes ( Sr/ Sr) are indicative of experi- the analysis because examination showed that the laser enced water salinity [35,45]. In preparation for analysis, transect did not traverse the primordium due to sample one sagittal otolith from each fish was embedded in two- preparation issues. An algorithm was used to consistently part epoxy resin (EpoFix; Struers, Ballerup, Denmark) and Partial migration drives subsidy allocation  43 determine the timing of freshwater entry based on the to ensure that the model was biologically relevant [52]. We 87 86 Sr/ Sr transect data for each fish following three criteria: used those relationships to back-calculate the length and 87 86 (i) Sr/ Sr ratio above 0.7096, corresponding to a salinity weight of fish at freshwater entry. We identified migration !" of <5 g.L in both rivers [23,35]; (ii) a local increase of to brackish water by visually identifying portions of the 87 86 87 86 Sr/ Sr ratio corresponding to a migration into less saline Sr/ Sr transects that were below or close to the value of 87 86 water; (iii) and an increase in the Sr/ Sr ratio (>2‰ / 50 0.7096 (Fig. 2). This value corresponds to a salinity of at -1 µm of transect) indicating sustained fresh water residence least 5 g.L during the wet season, according to previous (Fig. 2). We examined the relationship between otolith sampling and mixing models in the DR [35], and the SAR 87 86 core-to-edge transect distance and fish SL (mm) and [23]. In both rivers, Sr/ Sr show little change above 2 -1 87 86 weight (g) with least squared regression, assuming linear g.L , and a sharp decrease in otolith Sr/ Sr is indicative and log-linear relationship, respectively, in this range of a transition to brackish waters. of size (Additional material: Fig.S3, R² = 0.76) [51]. The analysis included a broad range of fish size (88-375 mm SL) A B Timor sea South Alligator River Daly River Gulf of NORTHERN Carpentaria TERRITORIES Australia C E D F Figure 1: (A) Map of the study area. (B) Zoom in the South Alligator River, orange circles show acoustic antenna locations, down to the estuary. (C) Aerial photography of the South Alligator River. (D) Photography of Planiliza ordensis, (E) shows the surgical implantation of an acoustic transmitter. (F) Example of a core-to-edge otolith transect. Diamonds show the location of annual rings. 44  Saboret et al. 2.3 Individual survival based on population ble and averaged 77 m (±48 SD) in length (range = 5–263 m). At the completion of each electrofishing shot, fish survey were counted and measured (SL) to the nearest mm, and As part of another study, 929 P. ordensis were surveyed returned alive to the point of capture. biannually in both the early and late dry season, over a We used length data to ensure that the back-calcu- 7-year period from 2006–2012 in the DR catchment. A lated size at freshwater entry determined by otolith micro- complete description can be found in Keller et al. 2019. chemistry was consistent with field data. We also used In brief, fish were sampled at discrete multiple locations those data to infer mortality in fresh water. As length did (shots or replicates) using a boat or backpack electrofish- not significantly differ between years (see Results), this ing (pulsed DC), depending on water depth. Electrofisher effect was not further considered. We used the von Ber- settings were adjusted to maximise efficiency of collect- talanffy equation that we established with otolith ageing ing fish with minimum power. At least 15 electrofishing (see above) as an age-length key to transform fish length shots of five minute elapsed duration were undertaken for to age and estimate population age structure [55]. As the each sampling event, and shots were stratified to ensure size structure did not differ between early and late dry each available habitat type within each site was sampled season (see Results), we pooled all age data by normaliz- at least once. Prior examination of sampling efficiency ing age structure to early dry season. We assumed that fish has revealed that 15 shots yields an accurate estimate of under 2 years were under-estimated due to sampling bias; species composition and assemblage structure within thus, we calculated disappearance for fish >2 years as the each site (Kennard et al. unpubl. data). Electrofishing proportion of fish missing between an age class and the shots were conducted in as homogenous area as possi- subsequent one. A B C D E F Core-to-edge distance (µm) Figure 2: Example of core-to-edge transect of otolith 87Sr/86Sr in individual P. ordensis from the Daly River (A-D) and South Alligator River (E-F). Blue dotted lines show the marine value of 87Sr/86Sr. Black diamonds show the location of annual increments. Green triangles show the predicted location of freshwater entry (see Methods). The two stars show example of seaward spawning migrations. 87 86 Srൗ Sr Partial migration drives subsidy allocation  45 2.4 Adult spawning behaviour and mortality test, we checked normality of data (Shapiro-Wilk tests and Q-Q plots). from acoustic tracking Data from 25 P. ordensis that were tracked in the SAR using acoustic telemetry were used to directly monitor 2.6 Allocation of subsidy modelling movements of fish into the putative spawning grounds and derive a second, independent mortality rate estimate We modelled the mean net biomass flux to freshwater that for comparison with the estimate from population age was driven by an individual P. ordensis, using an individ- structure [56]. Fish were collected by boat electrofishing ual mass balance approach, considering biomass that was and tagged by surgically implanting acoustic transmit- acquired in one biome and delivered to the other biome. ters (Vemco V13, 36 mm length, 11 g, 695 days estimated Given that diamond mullet mature in freshwater [37] and battery life, Vemco, Nova Scotia). Fish were adults, that movement in the marine environment is limited (see between 300-370 mm standard length (SL), mean 336 (±21 Results), we considered that most of biomass was delivered SD) mm SL. A complete description of the tagging method in the form of prey. Therefore, we only considered subsidy is provided by [23]. in the form of fish biomass as prey or carcasses for scav- An array of 30 acoustic receivers was deployed from engers (i.e. did not consider excretions), and considered the freshwater reaches of the SAR to the estuary mouth that fish disappearance was indicative of predation given (Fig. 1). As detections of all fish were contained within the high abundance of predators and scavengers in the the region covered by the acoustic receiver array, disap- system. The model only considered the delivery of alloch- pearance of telemetered fish within the battery life of the thonous biomass, therefore not considering juveniles transmitters was assumed to reflect mortality [57]. The that never migrated to fresh water and freshwater-derived sudden cessation of detection is a strong indicator of mor- biomass of fish that died in the river, which corresponds tality [58], as the only alternative hypothesis would be tag to organic matter turnover. We assumed negligible effects expulsion (which usually occurs shortly after tagging [59]) of growing during spawning residence in the marine envi- or tag malfunctioning (which is not expected [60]). ronment, meaning that marine-derived biomass was only We calculated the mortality rate using a full year of acquired before freshwater entry. We defined the freshwa- th th acoustic data from October 20 2013 to October 20 2014. ter-marine ecotone as the limit between inland water and Survival was computed using the function survfit in the the estuary. package survival [61], using the tsiatis method to estimate Thereby, net subsidy into fresh water (S) was calcu- survival error [62]. Ten of the 25 tagged mullet were not lated as the difference between the flux of marine-de- detected during the study, suggesting mortality in the rived biomass of fish dying in freshwater (Φf) and the immediate post-tagging period; possibly due to the relative flux of freshwater-derived biomass of spawners dying sensitivity of the species to handling and the harsh envi- in seawater (Φs): ronmental conditions at the time of collection and tagging -1 (water temperature >34°C, dissolved oxygen <1 mgL ). The (2) S =Φf– Φs, remaining 15 fish exhibited wide-ranging movements and we assume there were no long-term tagging effects for With Φf corresponding to the mass at freshwater entry these fish [63]. One fish was last detected at the furthest (𝑊𝑊 ) that is effecti vely delivered to fresh water by !"#$%& upstream antenna, and thus we could not determine its fish that die in freshwater, and can be defined as a fate and we did not include it in the survival analysis. gross subsidy into freshwater: 0* (3) 𝛷𝛷𝛷𝛷 = $ 𝑃𝑃 (𝑡𝑡 ) .𝑃𝑃 (𝑡𝑡 ) .(1− 𝑃𝑃 (𝑡𝑡 ) ).𝑊𝑊 𝑑𝑑𝑡𝑡 !"#$% #'()" *(+,#$(-+ ."-$,/ 0."-$,/ 2.5 Statistical analysis And Φs corresponding to the mass derived from freshwa- All data analysis, statistics and modelling were done in R ter that is effectively delivered to seawater by spawners version 4.0.2 [64]. that do not return from spawning: To test for effect of sex on skipped spawning rates, 0* 𝛷𝛷𝛷𝛷 = $ 𝑃𝑃 (𝑡𝑡 ) .𝑃𝑃 (𝑡𝑡 ) .𝑃𝑃 (𝑡𝑡 ) .(𝑊𝑊 (𝑡𝑡 )−𝑊𝑊 ) 𝑑𝑑𝑡𝑡 effect of sex and size on weight-to-length relationship (4) !"#$% #'()" *(+,#$(-+ ."-$,/ residuals, and effect of seasons and years on age fre- quency, we performed one-way ANOVA tests. For each 46  Saboret et al. 3 Results 𝑃𝑃 (𝑡𝑡 ) 𝑃𝑃 (𝑡𝑡 ) 𝑃𝑃 (𝑡𝑡 ) 𝑊𝑊 (𝑡𝑡 ) !"#$% !"#$% !"#$%&"'# , , and are the probability of dying, being alive, migrating (i.e. being in seawater), and weight at age t, respectively. Tfentry, Tf and 3.1 Migratory patterns of P. ordensis Tm are the age at freshwater entry, first and last spawning 𝑊𝑊 !"#$%& migration, respectively. is the weight at freshwa- Estimated fish ages ranged from 1 to 6 years, with a ter entry, which corresponds to the biomass derived from mean of 2.9 years (SD=0.9). In the DR, the seasonal 87 86 seawater.. oscillations in Sr/ Sr ratio between 0.72 and 0.73 We assumed that mortality was independent of time (characteristic of the main channel, see [35]) matched 87 86 of the year, age and habitat (see Results). Therefore, S was with annual increments and Sr/ Sr in between the pri- simply calculated as: mordium and the first increment were very close to the marine value of 0.70907 [67], confirming marine resi- (5) dence in the juvenile phase and catadromy (e.g. Fig. 2). Of the 68 fish examined, 66 (97%) showed a clear tran- 87 86 𝑃𝑃 Where ss is the skipped spawning rate, is the sition in otolith Sr/ Sr from marine to fresh water (Fig. !"#$% annual mortality and Δt the time spent in the estuary. 2). The two fish which did not exhibit such a transition The equation corresponds simply to the marine-derived were small fish (<125 mm SL) and had likely migrated biomass that is imported into fresh water by migrating into fresh water just prior to capture, leaving insuffi- 𝑊𝑊 (𝑡𝑡 ) juveniles ( ) subtracted by the biomass that cient time for incorporation of the freshwater chemical 𝑊𝑊 !"#$%& is exported by spawners (1−𝑠𝑠𝑠𝑠 ) that are still alive at signature (see [68]); in these cases the core-to-edge dis- $'( 𝑃𝑃 time t ((1−𝑃𝑃 ) ) and die in the estuary ( Δt ), tance was taken as freshwater entry. Age at freshwater !"#$% !"#$% throughout life of adult fish (integral from Tf to Tm). The entry ranged between 0+ year (44% of individuals) and equation was computed numerically using a daily incre- 1+ year (56%). Back-calculated SL at freshwater entry ment. Table 1 summarizes how the different parameters was normally distributed (Shapiro-Wilk test, W-statis- have been inferred. tic=0.98, P=0.39), with a mean of 147 mm (SD=26) (Fig. 3A). This corresponded to an individual mass of an average 72.8g ([62.8, 82.8] 95% CI). Length-frequency 2.7 Model extension to other diadromous data were consistent with the estimated size at fresh- water entry from otolith back-calculation, with only fishes two fish <90 mm SL recorded from freshwater (Fig. 3C). The model was used to investigate how migratory behav- Otolith chemistry revealed few migrations into the iour (age at first migration and skipped spawning) of other marine environment (14 % of fish between 2 and 3 years diadromous fishes might affect nutrient fluxes, in relation N=43, 0% of fish beyond 3 years N=9; Fig. 2A, C). The to annual mortality and growth coefficient, two parame- acoustic telemetry showed that five of the 10 fish still ters which are subject to broad variations among systems being tracked after the late wet season had migrated due to external influences [65,66]. The model extension downstream into the putative spawning grounds down- is based on the premise that diadromous fishes use one stream the lower estuary (Fig. 4A). Residence times of biome for growth, and the other biome to spawn and some migrating fish in the lower estuary were very short grow as early juveniles, therefore excluding feeding in the (only a few days), which may explain the lower number of spawning biome and omitting excretions in the spawning migrations detected by otolith chemistry analysis: short- biome for simplification. For the purposes of this explor- term migrations can be difficult to detect using otolith atory modelling exercise, key life history traits were held chemistry due to the laser spot size and time taken for at the same value (maximal age fixed at 10 years; maximal otolith chemistry to reach equilibrium with the ambient weight fixed at 10 kg; same growth model (equation (1)); water [68]. Nonetheless, both the otolith chemistry and constant mortality) so that predicted subsidy differences acoustic tracking data suggested a high proportion of only reflect migration behaviour differences. skipped spawning each year. Altogether, our data showed a high skipped-spawning rate (~50% and 85% from telem- etry and otolith chemistry, respectively) and for the pur- poses of modelling, we used an annual skipped spawning rate of 50% for P. ordensis (Table 1). We also assumed that fish spent an average of 4 months in the estuary based on Partial migration drives subsidy allocation 47 our telemetry and otolith data, and previous studies [34] beyond 2 years [35], supporting that disappearance was (Table 1). Although sample size was low (n=35), the otolith reflective of mortality. chemistry data suggested no bias in skipped spawn- Tagged fish were detected frequently by the passive ing rates among sexes for mature individuals (one-way acoustic receiver array, with average delays between ANOVA, F = 0.09, P = 0.76). detections of 2.5 hours and the maximum time between detections averaging 41 days (min = 1 d, max = 110 d). This frequency of tag detection, the lack of detections on 3.2 Mortality of P. ordensis the most downstream loggers in the system for most fish, and the estimated tag battery life of ~2 years, all support Age frequency data for the DR did not differ between years our assumption that fish that were undetected for >1 year (one-way ANOVA, F = 1.84, P = 0.2) and seasons (Fig. 3C, had suffered mortality within the system. The acoustic one-way ANOVA, F = 0.63, P = 0.46), and thus was mod- tracking showed a relatively constant rate of decrease elled as an age-independent disappearance rate of ~60% in the number of tagged individuals detected through- 87 86 for fish > 2 years of age (Fig. 3D). Otolith Sr/ Sr ratio sig- out the year (Fig. 4B), suggesting that time of the year natures in the same system suggested that no emigration (i.e., seasons) did not strongly affect the mortality rate. from another system (such as tributaries) occurred for fish Although the number of individuals was low, estimates of annual mortality from the acoustic telemetry were high A B Figure 3: (A) Distribution of back-calculated length at freshwater entry of P. ordensis. Blue line shows the normal distribution of the data. (B) Distribution of back-calculated weight at freshwater entry of P. ordensis. Blue line shows the normal distribution of the data. (C) Length distribution of P. ordensis from the Daly River, obtained by biannual sampling in 2012 (King A., unpub. data.). Blue line shows the mean back-calculated length at freshwater entry. (D) Age structure of P. ordensis >2 years. Open circles show the calculated disappearance rate between age classes. Bars show 95% confidence interval of disappearance rate. 48   Saboret et al. the low proportion of migrating individuals (i.e. skipped spawning). Skipped spawning was a strong factor affect- ing subsidy allocation. For an annual skipped spawning rate of 50% -which appears realistic in this population, see above-, we estimated that each mullet represented a net 42.8g flux into fresh water (Fig. 5). However, absence of skipped spawning would result in near-null balance of fluxes with almost as much biomass exported as imported in freshwater (net flux to fresh water of just 12g). 3.4 Predictions for other diadromous fishes Extending the model to other life-history traits showed that catadromous fishes could allocate a net biomass flux to either marine or freshwater habitat (Fig. 6). Skipped spawning rate was an important driver of the allocation. Populations with low skipped-spawning rate (i.e. most of individuals migrate every year) could only represent a net flux into fresh water under high mortality that prevented most of individuals from growing to large size and export- ing biomass when migrating to spawn. In populations with high skipped-spawning rates, the export of biomass remained limited, generally resulting in a net subsidy for Figure 4: Acoustic telemetry tracking of 15 P. ordensis over one freshwater ecosystems. In that case, the magnitude of the year in the South Alligator River. (A) Survival estimate against time. subsidy depended mostly on the mass at freshwater entry, Dashed line denotes 95% confidence estimate. (B) Location of detection events, each colour showing one individual. Stars (on the which was determined by growth and age at freshwater right) show the locations of acoustic antennas. Crosses show esti- entry, while mortality had limited influence because most mated fish death (loss of record, see Methods). Question mark “?” of individuals died while in freshwater. denotes uncertain fate of the fish (death or upstream migration). Given that catadromous and anadromous fishes are broadly symmetrical, the direction of the biomass flux at around 80% ([0.45, 0.96] 95% CI) which overlapped was inverted in the case of anadromous fish. Populations with the estimate from age structure. Altogether, our data of anadromous fish with high skipped-spawning rates suggest a relatively constant, age- and habitat-independ- could only act as a net import of biomass to fresh water ent mortality rate of approximatively 60-80% per year if juveniles migrate early to the seawater, growth fast in (Table 1). the marine environment and there is high survival (Fig. 6). 3.3 Allocation of subsidies 4 Discussion The maximum subsidy per individual to fresh water cor- responded to the mass at fresh water entry ~72 g that was 4.1 Prevalence of skipped spawning estimated from otolith back-calculation and supported by population survey data (Fig. 5). Before the first spawning There is growing evidence that migration is a highly migration, 80% of this flux was effectively delivered to variable phenomenon at the individual level [69], and freshwater food webs due to high mortality, corresponding Thomson noted many decades ago that populations of a to gross flux to fresh water. Despite the fact that mature catadromous mullet, Mugil cephalus, were composed of individuals weigh much more that juveniles at fresh water individuals forgoing seaward spawning migration [70]. entry, the flux from fresh water to seawater was damp- Otolith microchemistry further confirmed high prevalence ened by the low survival, the relatively high probability of skipped spawning in M.cephalus with some individuals for adults to return to fresh water (i.e. iteroparity) and staying in fresh water for extended periods (>7 years) [71]. Relative survival Partial migration drives subsidy allocation 49 Table 1: Parameter estimates used to model nutrient fluxes in the study. Parameter Estimate Parameter (Equation) Method Length-weight relationship log(a)=-11.0, b=3.05 a, b (1) Fish collection Size parameter 0.32 l (1) Otolith ageing Growth rate 0.332 K (1) Otolith ageing Maximum length 500.1 mm SL (1) Otolith ageing max Weight at freshwater entry 72.8g W (5) Otolith microchemistry, fish survey fentry Age at first spawning 2 years T (5) Otolith microchemistry, acoustic telemetry Maximum age 7 years T (5) Fish survey -1 Mortality rate 0.6. year P(t) (5) Fish survey, Acoustic telemetry death Time in the estuary 4 months Δt (5) Acoustic telemetry Skipped spawning rate ~50% ss (5) Otolith microchemistry, Acoustic telemetry A B Seawater Fresh water Cumulative net flux in fresh water (g/individual) Migrant ɸf Juvenile Freshwater ~1 year entry Larva Maturity >2 years Eggs migration Weight x8 Skipped Survival 21% spawning Fish age (years) ɸf-ɸs migration Skipped spawning ɸs Weight x28 Survival 0,6% Skipped 0% 50% Spawning: Figure 5: (A) Life history of P. ordensis, as inferred from otolith microchemistry, age-at-length data and acoustic telemetry. Φf (Flux into fresh water, blue arrow) and Φs (Flux into seawater, green arrows) represent the flux of biomass across the freshwater-marine ecotone, as calculated in equation (3) and (4). (B) Dashed line: relative survival after freshwater entry, dotted line: relative weight, continuous line: net cumulative flux in fresh water. After freshwater entry, migrating juveniles start to be preyed in the river resulting in a positive net cumulative flux from the marine to the freshwater environment. Before the first spawning migration, around 80% of mullets have been preyed, meaning that 80% of the mass at freshwater entry (73 g) has been delivered to the river food web. After maturation, the flux is inverted as individuals start to migrate and some do not return from seawater. Older individuals contribute relatively less to fluxes as the increase in biomass is out- weighed by the decrease in survival, given our parameters. With increasing proportion of individuals migrating (skipped spawning from 0% to 50%), fluxes to seawater proportionally increase. The net flux of subsidies into fresh water is the cumulative net flux at final age, which is the sum of a continuous incoming flux after freshwater entry -as all individuals derive some mass from their marine phase- and outgoing fluxes at spawning migration –driven by much fewer individuals of bigger mass. Age at first migration 1,2 0,8 1 50   Saboret et al. Skipped spawning Average subsidy 20% 50% 80% per individual (%/total mass) 0.55 into fresh water 0.45 0.35 0.25 0.55 0.45 0.35 0.25 0.55 -5 0.45 0.35 -10 0.25 0.2 0.4 0.6 0.8 0.2 0.4 0.6 0.8 0.2 0.4 0.6 0.8 -15 Mortality Mortality Mortality Figure 6: Modelling of the allocation of subsidies across the freshwater-marine ecotone driven by an iteroparous catadromous fish, accor- ding to intra-variation life history (see Methods). Skipped spawning increases from the left to the right and age at first migration from the top to the bottom. For a given skipped spawning and age at first migration (i.e. within an individual square), mortality increases from the left to the right and growth from the bottom to the top. Shade of colour shows the direction and magnitude of subsidy in fresh water (kg) for a hypothetic fish that could reach 10 kg at a maximum age of 10 years (see legends). Given that catadromous and anadromous fishes play sym- metrical roles, the direction of the biomass flux is simply inverted in the case of an iteroparous anadromous fish. In line with these studies, our study of P. ordensis showed tion of post-spawned individuals by otolith microchemis- that only a subset of mature individuals migrated every try (i.e. some fish survived spawning migration). In both year to the spawning grounds. Skipped spawning can be cases, telemetry suggested that most fish are preyed upon explained by a trade-off between the benefit and cost of in fresh water before they reach the estuarine spawning spawning over the long term, as individuals can maxi- grounds. mize their cumulative reproductive output by skipping breeding, reducing mortality risk and devoting resources towards growth [24,25]. P. ordensis is a capital breeder (i.e. 4.2 Net import of biomass driven by P. store energy for latter reproduction [72]) which accumu- ordensis lates fat during the wet season in productive floodplains and allocates this energy for reproduction during the To our knowledge, this study is the first estimate of the dry season [37]. In the case of migratory fishes, skipped direction of biomass fluxes driven by a catadromous fish spawning might be especially common because of the across the freshwater-marine ecotone. Using an individual mortality risk and energetic costs associated with migra- mass-balance approach, we showed that skipped spawn- tion [26]. In our study, we could not clearly conclude from ing dampened the flux of biomass to the sea, resulting in a telemetry if mortality was higher for migrants because net subsidy of on average ~43 g to freshwater ecosystems. some individuals could move downstream without the This magnitude of subsidy is likely to be important at the intention of breeding. The estimated annual mortality rate ecosystem level as P. ordensis is a common prey species of ~60% and the observation of high mortality outside the for high-order predators in Northern Australian Rivers migration period suggest that either very few individuals [33,38], and given observations of massive schools of migrate at high mortality cost, or that the mortality cost mullet entering fresh water (authors pers obs.). The alloca- of migration is low, which is supported by the observa- tion of prey to one or another habitat can have bottom-up Growth Growth Growth Partial migration drives subsidy allocation  51 effects on predators [30], with far-reaching consequences requirements of this species to migrate from freshwater to on ecosystem functioning [73]. This input of marine-de- marine spawning grounds, one might predict that barra- rived biomass could carry essential nutrients and energy mundi acts as a net export of energy to the sea. However, to sustain high productivity in those ecosystems while this species also shows a high variability of migratory being limited in nutrients most of the year [42]. Even small strategies [81], including a high prevalence of skipped subsidies can play a critical role in ecosystem processes. spawning [23], which our model suggest may invert the For instance, the migration of mayflies can increase juve- source-sink coupling between marine and freshwater eco- nile salmon growth in a one-to-three ratio and sustain in systems. cool tributaries populations of fish that are key ecosystem We expect that the predictions of our models may engineers [74]. apply to other diadromous fishes. However, it is worth Although our study only considers the net direction noting that our model only considers subsidies in the form of fluxes to identify source and sink across the freshwater- of fish biomass and might not apply to specificities of other marine ecotone, it should be recognised that the potential life histories [82]. Some fish, such as Atlantic salmons, effect of subsidies also relies on the quality of energy consume most of their energy reserves (up to 70%) for long [75] and delivery pathways within food-webs [76,77]. For distance migration, maturation and sexual development instance, marine subsidies can be critical for freshwater [83]. By doing so, fish contribute subsidies in the form of ecosystems because of their role in supplying high quality excreted nutrients in the spawning habitat. For instance, fatty acids [78] or micronutrients [79], rather than simple anadromous shad lose ~30% of weight while migrating mass-balance processes. Our study also only focused on from the marine environment into rivers [84]. However, the fluxes between seawater and fresh water, but it is nutrients that are excreted in the growing habitat (e.g., worth noting that P. ordensis also contribute to moving energy reserve consumed by salmons in the ocean) do not energy within those biomes. Despite the fact that juvenile contribute to biomass flux across the freshwater-marine growth appears to occur in seawater, adults might spawn ecotone as they represent turnover of autochthonous (i.e. and be preyed in the intertidal zone. Within the river, formed where it is found) organic matter. growth could be supported by terrestrial carbon [40] While our model contains several simplifications, and be allocated in other reaches of the streams [54], or we believe it has potential utility as a framework in many even return to terrestrial ecosystems via predation by cases to examine the allocation of biomass by diadromous birds. Therefore, although the study focused on fluxes fishes. For example, iteropareous Atlantic salmon (Salmo across the freshwater-marine ecotone, it is worth noting salar) are usually considered as transporters of energy that diadromous fish like P. ordensis may also transport and nutrients to streams [85,86]. However, they also show biomass within and into other biomes. high variability in reproductive strategy [87], with some populations composed of only ~5% repetitive spawners [88]. Thus, despite the high ratio of adult:juvenile mass, 4.3 Revisiting the role of diadromous fishes we suspect that iteroparous anadromous salmonids, such as Atlantic salmon, could in some instances act as on the allocation of subsidies across the an export of energy to the sea in populations where when freshwater-marine ecotone skipped spawning is common. This prediction is in line Contrary to expectations [18], our model predicted that with historical estimates showing that even semelparous fresh water may act as a sink of marine-derived biomass Pacific salmon (Oncorhynchus spp.) could act as a net flux driven by a catadromous fish. Given the very high abun- of nutrients to the sea when the proportion of returners is dance of P. ordensis and other catadromous species, such low [89]. as barramundi, Lates calcarifer, tarpon, Megalops cypri- This inversion of nutrient flux was also explained by noides, and other mugilids across northern Australia, we a nonlinear relationship between spawner abundance extended our model to other life-history traits. The exten- and the number of migrating smolts [90], illustrating sion of the model shows that when considering skipped that density dependence processes may drive feed-backs spawning, catadromous fishes are much more likely to act between fish life-history (e.g. the proportion of spawners) as a net biomass flux to fresh water. For instance, barra- and biomass fluxes. In addition, while the direction of mundi are characterized by relatively rapid growth [80], subsidies is determined by individual life history, the mag- high ratio (>10) between mass at spawning and at fresh- nitude also depends on population dynamics. Increased water entry, and relatively higher survival than P. orden- skipped spawning by P. ordensis results in retention of sis based on telemetry and ageing [23]. Considering the biomass in fresh water, but could also decrease the total 52   Saboret et al. amount of subsidies over the long term, as fewer indi- Kakadu National Park research permits RK786, RK805 and viduals spawn, resulting in lower biomass flux of juve- RK862. niles. In turn, skipped spawning is a conditional strategy in fish [22,24] that is strongly affected by environmental conditions. More studies are needed to integrate the rela- Acknowledgements tionship between the import and export of biomass in dynamic systems, and the implications for subsidy stabil- We gratefully acknowledge traditional indigenous owners ity with regards to environmental variation. of those parts of the South Alligator River (the Bininj and Mungguy people) and the Daly River (the Wardaman, Jawoyn, Wagiman and Malak Malak people) in which this study took place, and thank them for providing access 5 Conclusion to their land. Anne O’Dea (Parks Australia) coordinated Indigenous consultation within Kakadu National Park The model derived in this study offers a simple tool to and provided assistance with logistics and field activities. examine subsidy allocation across the freshwater-ma- Staff from the Department of Industry, Tourism and rine ecotone by diadromous fishes. We show that skipped Trade (NT Fisheries), in particular Quentin Allsop and spawning in a catadromous fish can lead to a net import Wayne Baldwin, are thanked for assistance with the of subsidies in freshwater ecosystems. Furthermore, we collection of fish. Peter Kyne led the set-up, maintenance highlight that variation in migratory behaviour in other and downloading of the acoustic telemetry array. We diadromous fishes could affect the source-sink coupling gratefully acknowledge John Woodhead, Roland Maas between the ocean and inland waters. Fish migration and Alan Greig (University of Melbourne) for assistance behaviours are affected by recent human disturbances, with the otolith chemistry analysis. Fish samples were such as artificial barriers [91], global warming [92] and obtained from the Daly River Fish Monitoring Project, with fishing pressure [93]. The tropical river systems of Austral- financial support from Charles Darwin University and the ia’s north are not exempt from environmental threats and Northern Territory Government. Funding for this research our study highlights that conservation effort should be was provided by the Australian Government’s National directed towards protecting connectivity between rivers Environmental Research Program. GS was supported by an and the sea to preserve the integrity of energetic fluxes international internship from Ecole Normale Supérieure across ecotone boundaries. de Lyon, France. Author contribution References DC, MD and AK designed the study. DC, DB, AK and MD [1] Loreau M, Holt RD. Spatial Flows and the Regulation of collected the data. GS and DC analysed the data. GS led Ecosystems. Am Nat. 2004;163:606–15. the writing of the manuscript with substantial input from [2] Polis GA, Wendy B. Anderson1, and, Holt RD. TOWARD AN DC. 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Journal

Animal Migrationde Gruyter

Published: Jan 1, 2021

Keywords: Partial migration; Skipped spawning; Catadromy; Marine-derived nutrients; Prey availability

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