Identifying the interacting roles of stressors in driving the global loss of canopy‐forming to mat‐forming algae in marine ecosystems

Identifying the type and strength of interactions between local anthropogenic and other stressors can help to set achievable management targets for degraded marine ecosystems and support their resilience by identifying local actions. We undertook a meta‐analysis, using data from 118 studies to test the hypothesis that ongoing global declines in the dominant habitat along temperate rocky coastlines, forests of canopy‐forming algae and/or their replacement by mat‐forming algae are driven by the nonadditive interactions between local anthropogenic stressors that can be addressed through management actions (fishing, heavy metal pollution, nutrient enrichment and high sediment loads) and other stressors (presence of competitors or grazers, removal of canopy algae, limiting or excessive light, low or high salinity, increasing temperature, high wave exposure and high UV or CO₂), not as easily amenable to management actions. In general, the cumulative effects of local anthropogenic and other stressors had negative effects on the growth and survival of canopy‐forming algae. Conversely, the growth or survival of mat‐forming algae was either unaffected or significantly enhanced by the same pairs of stressors. Contrary to our predictions, the majority of interactions between stressors were additive. There were however synergistic interactions between nutrient enrichment and heavy metals, the presence of competitors, low light and increasing temperature, leading to amplified negative effects on canopy‐forming algae. There were also synergistic interactions between nutrient enrichment and increasing CO₂ and temperature leading to amplified positive effects on mat‐forming algae. Our review of the current literature shows that management of nutrient levels, rather than fishing, heavy metal pollution or high sediment loads, would provide the greatest opportunity for preventing the shift from canopy to mat‐forming algae, particularly in enclosed bays or estuaries because of the higher prevalence of synergistic interactions between nutrient enrichment with other local and global stressors, and as such it should be prioritized.     

Decadal losses of canopy‐forming algae along the warm temperate coastline of Brazil

The loss of canopy‐forming seaweeds from urbanized coasts has intensified in response to warming seas and non‐climatic pressures such as population growth and declining water quality. Surprisingly, there has been little information on the extent of historical losses in the South‐western Atlantic, which limits our ability to place this large marine ecosystem in a global context. Here, we use meta‐analysis to examine long‐term (1969–2017) changes to the cover and biomass of Sargassum spp. and structurally simple algal turfs along more than 1,000 kilometres of Brazil's warm temperate coastline. Analysis revealed major declines in canopy cover that were independent of season (i.e., displaying similar trends for both summer and winter) but varied with coastal environmental setting, whereby sheltered bays experienced greater losses than coastal locations. On average, covers of Sargassum spp. declined by 2.6% per year, to show overall losses of 52% since records began (ranging from 20% to 89%). This contrasted with increases in the cover of filamentous turfs (24% over the last 27 years) which are known to proliferate along human‐impacted coasts. To test the relative influence of climatic versus non‐climatic factors as drivers of this apparent canopy‐to‐turf shift, we examined how well regional warming trends (decadal changes to sea surface temperature) and local proxies of coastal urbanization (population density, thermal pollution, turbidity and nutrient inputs) were able to predict the changes in seaweed communities. Our results revealed that the most pronounced canopy losses over the past 50 years were at sites exhibiting the greatest degree of coastal warming, the highest population growth and those located in semi‐enclosed sheltered bays. These findings contribute knowledge on the drivers of canopy loss in the South‐western Atlantic and join with global efforts to understand and mitigate declines of marine keystone species.     

Dominant (AFLP) and co‐dominant (microsatellite) markers for the kelp Postelsia palmaeformis (Laminariales)

To aid in understanding the structure, dispersal and genetic dynamics of their populations, we developed microsatellite and amplified fragment length polymorphism (AFLP) markers for the sea palm, Postelsia palmaeformis (Laminariales) for samples taken from nine sites in the area of Cape Flattery, Washington State, USA. We identified two AFLP primers that yielded 798 variable fragments and five microsatellite markers with three to seven alleles each. We also report patterns of allelic variation for four previously identified microsatellite markers in this species and several new alleles.     

Climate‐driven substitution of habitat‐forming species leads to reduced biodiversity within a temperate marine community

Aim

In marine ecosystems, habitat‐forming species (HFS) such as reef‐building corals and canopy‐forming macroalgae alter local environmental conditions and can promote biodiversity by providing biogenic living space for a vast array of associated organisms. We examined community‐level impacts of observed climate‐driven shifts in the relative abundances of two superficially similar HFS, the warm‐water kelp Laminaria ochroleuca and the cool‐water kelp Laminaria hyperborea.

Location

Western English Channel, north‐east Atlantic

Methods

We compared algal and invertebrate assemblages associated with kelp stipes and holdfasts, across multiple sites and sampling events. Significant differences were recorded in the structure of assemblages between the host kelp species at each site and event.

Results

Assemblages associated with stipes of the cool‐water HFS were, on average, >12 times more diverse and supported >3600 times more biomass compared with the warm‐water HFS. Holdfast assemblages also differed significantly between species, although to a lesser extent than those associated with stipes. Overall, assemblages associated with the warm‐water HFS were markedly impoverished and comprised far fewer rare or unique taxa.

Main conclusions

While previous research has shown how climate‐driven loss of HFS can cause biodiversity loss, our study demonstrates that climate‐driven substitutions of HFS can also lead to impoverished assemblages. The indirect effects of climate change remain poorly resolved, but shifts in the distributions and abundances of HFS may invoke widespread ecological change, especially in marine ecosystems where facilitative interactions are particularly strong.     

Spatial patterns of self‐recruitment of a coral reef fish in relation to island‐scale retention mechanisms

Oceanographic features influence the transport and delivery of marine larvae, and physical retention mechanisms, such as eddies, can enhance self‐recruitment (i.e. the return of larvae to their natal population). Knowledge of exact locations of hatching (origin) and settlement (arrival) of larvae of reef animals provides a means to compare observed patterns of self‐recruitment ‘connectivity’ with those expected from water circulation patterns. Using parentage inference based on multiple sampling years in Moorea, French Polynesia, we describe spatial and temporal variation in self‐recruitment of the anemonefish Amphiprion chrysopterus, evaluate the consistency of net dispersal distances of self‐recruits against the null expectation of passive particle dispersal and test the hypothesis that larvae originating in certain reef habitats (lagoons and passes) would be retained and thus more likely to self‐recruit than those originating on the outer (fore) reef. Estimates of known self‐recruitment were consistent across the sampling years (~25–27% of sampled recruits). For most (88%) of these self‐recruits, the net distance between hatching and settlement locations was within the maximum dispersal distance expected for a neutrally buoyant passive particle based on the longest duration of the larval dispersive phase and the average direction and speed of current flow around Moorea. Furthermore, a parent of a given body size on the outer (fore) reef of Moorea was less likely to produce self‐recruits than those in passes. Our findings show that even a simple dispersal model based on net average flow and direction of alongshore currents can provide insight into landscape‐scale retention patterns of reef fishes.     

Influence of sedimentation in the absence of macrograzers on recruitment of an annual population of Macrocystis pyrifera in Metri Bay,Chile

The effects of sedimentation and substrate orientation on algal and sessile invertebrate assemblages were tested on an annual population of Macrocystis pyrifera in Metri Bay, southern Chile. In the laboratory, M. pyrifera zoospores were seeded on Crepipatella fecunda shells, the primary substrate for M. pyrifera in this system. The seeded shells were deployed at Metri Bay inside cages and were orientated vertically and horizontally under two sedimentation regimes (bottom and suspended). Due to differences in grazer accessibility and the species present between the sedimentation treatments, grazers (>1 cm) were excluded. We followed sporophyte development of M. pyrifera and the natural recruitment of other algal and invertebrate species. Sedimentation rates were significantly higher in the cages attached to the bottom compared to suspended cages (P < 0.001). In total M. pyrifera and three additional algal genera were detected and all algal recruits showed significantly greater recruitment on the horizontally orientated substrate compared to the vertical substrate. Macrocystis pyrifera sporophytes were present only on the horizontal, suspended (less sedimentation) treatment. In contrast, Ulva and Ectocarpus spp. also occurred in the horizontal, high sediment treatment. Invertebrate recruitment (amphipods, barnacles and spirorbids) dominated the vertically oriented shells regardless of sedimentation. Results indicate that high sedimentation negatively affected the development of M. pyrifera sporophytes while other opportunistic species were able to recruit under these conditions.     

Positive interaction between invasive plants: The influence of Pyracantha angustifolia on the recruitment of native and exotic woody species

Abstract: Positive interactions between species are known to play an important role in the dynamics of plant communities, including the enhancement of invasions by exotics. We studied the influence of the invasive shrub Pyracantha angustifolia (Rosaceae) on the recruitment of native and exotic woody species in a secondary shrubland in central Argentina mountains. We recorded woody sapling recruitment and micro‐environmental conditions under the canopies of Pyracantha and the dominant native shrub Condalia montana (Rhamnaceae), and in the absence of shrub cover, considering these situations as three treatments. We found that native and exotic species richness were higher under Pyracantha than under the other treatments. Ligustrum lucidum (Oleaceae), an exotic bird‐dispersed shade‐tolerant tree, was the most abundant species recruiting in the area, and its density was four times higher under the canopy of Pyracantha. This positive interaction may be related to Pyracantha's denser shading, to the mechanical protection of its canopy against ungulates, and/or to the simultaneous fruit ripening of both woody invaders.     

Restoring depleted coral‐reef fish populations through recruitment enhancement: a proof of concept

To determine whether enhancing the survival of new recruits is a sensible target for the restorative management of depleted coral‐reef fish populations, settlement‐stage ambon damsel fish Pomacentrus amboinensis were captured, tagged and then either released immediately onto small artificial reefs or held in aquaria for 1 week prior to release. Holding conditions were varied to determine whether they affected survival of fish: half the fish were held in bare tanks (non‐enriched) and the other half in tanks containing coral and sand (enriched). Holding fish for this short period had a significantly positive effect on survivorship relative to the settlement‐stage treatment group that were released immediately. The enrichment of holding conditions made no appreciable difference on the survival of fish once released onto the reef. It did, however, have a positive effect on the survival of fish while in captivity, thus supporting the case for the provision of simple environmental enrichment in fish husbandry. Collecting and holding settlement‐stage fish for at least a week before release appear to increase the short‐term survival of released fish; whether it is an effective method for longer‐term enhancement of locally depleted coral‐reef fish populations will require further study.     

Empirical evidence for large‐scale human impact on intertidal aggregations,larval supply and recruitment of Pyura praeputialis around the Bay of Antofagasta,Chile

In northern Chile, Pyura praeputialis is an invasive species inhabiting rocky intertidal and subtidal habitats restricted exclusively to the Bay of Antofagasta where it forms extensive aggregations. The negative impact of Pyura gathering on mid‐intertidal abundances of this species has recently been reported at the south‐eastern end of this bay. In the present study we have increased sampling sites to cover the entire bay toward the north‐western end and the northern section, where a coastal marine reserve for the scallop fishery partially restricts shellfish gathering. Therefore, the sampling sites were chosen to represent different levels of shellfish gathering access along the northern shore of the bay. Long‐term monitoring (1999–2014) of changes in tunicate cover and the abundances of larvae and recruits at seven sites are reported. The opening of a remodelled artificial and recreational beach in 2012, on the central‐eastern shore of the bay, has increased accessibility to rocky intertidal platforms that started to be massively visited by Pyura gatherers from the summer of 2013. This allowed for the implementation of an intensive short‐term monitoring program of changes in tunicate cover and the abundances of their larvae and recruits. When gathering access was present the reduction in intertidal cover was generalized to the entire bay and followed by reductions in larvae and recruits. However, these reductions were not found in sites with more restricted gathering access. We conclude that continuous extraction by Pyura gatherers followed by reductions of conspecific larvae and recruits are the main drivers behind the reduced abundance of P. praeputialis in the entire bay of Antofagasta. Thus, if gathering is not stopped important ecosystem services provided by this tunicate in the bay may be threatened. Similar consequences may be expected if other massive and irreversible reductions in other species of the Pyura complex, that inhabit other coasts in the southern hemisphere, occur. The controversy concerning the impacts of invasive species and whether they cause negative, positive or neutral impacts to original ecosystems and fisheries is discussed.     

Isolation and characterization of nine polymorphic microsatellite loci of the kelp greenling, Hexagrammos decagrammus, a temperate reef fish

Nine polymorphic microsatellite loci were developed and characterized for the temperate reef fish species, Hexagrammos decagrammus (kelp greenling). The number of alleles varied from three to 22 in a sample of 22 individuals from one population. Expected heterozygosities ranged from 0.354 to 0.979. These microsatellites allow us to investigate reproductive success of individuals, alternative mating strategies as well as population structure and metapopulation dynamics of this species.     

Plant and frond dynamics of the giant kelp,Macrocystis pyrifera,forming a fringing zone in the Falkland Islands

Fluctuations in plant and frond characteristics are described for Macrocystis pyrifera (L.) C. Agardh (Laminariales, Phaeophyta) forming a fringing zone in the Falkland Islands. Giant kelp plants were sampled along a transect in the austral autumn (May 1986) and late spring (December 1986) which, according to previous frond weight analysis, were the times when extremes in population parameters were expected. Plant density and holdfast wet weights were similar for both seasons, but plants had more fronds and the fronds weighed more in spring than in autumn. Consequently, in autumn the frond biomass (1·1 wet kg m^?2) and productivity (34·1 wet g m^?2 d^?1) were lower than in spring, when a biomass of 5·0 wet kg m^?2 and a productivity of 72·4 wet g m^?2 d^?1 were recorded. Production of new fronds and loss of old fronds were determined at monthly intervals between April 1986 and March 1987. New frond production rates followed fluctuations in the quantity of light and varied between 0·08 and 0·48 fronds per plant per day. Frond loss rates did not show a seasonal pattern and fluctuated between 0·05 and 0·42 fronds per plant per day. It is suggested that the Falkland Islands Macrocystis population is more stable than most other giant kelp beds at high latitudes, because of the absence of winter storms.     

Long‐distance dispersal and local retention of larvae as mechanisms of recruitment in an island population of a coral reef fish

Abstract Although recruitment of pelagic larvae is a fundamental and well‐documented process in the dynamics of benthic marine populations, identifying the sources of recruitment, or the degree to which populations are connected via dispersal of larvae, has remained elusive for most marine taxa. In this study we used natural environmental markers (trace elements) recorded in fish otoliths (ear stones) as tags of natal origin. Specifically, we used the otolith core and edge chemistries of a locally endemic wrasse (Coris bulbifrons) from Lord Howe Island (LHI), Australia, and a widely distributed species (Coris picta) from three potential mainland source regions, to determine the likely sources of recruitment to C. picta populations on LHI. The use of a local endemic species, which is by definition self‐recruiting, is a novel approach for ground‐truthing the dispersal history of non‐endemic coral reef fish. Discriminant function analyses were able to separate LHI from mainland fish, using both edge and core signatures, with a high degree of accuracy, suggesting at least some of the C. picta collected on LHI were of local origin. This result was corroborated when half of the C. bulbifrons and LHI C. picta were introduced as unknowns into a discriminant function analysis using the remaining C. bulbifrons, LHI C. picta, and the mainland C. picta as a training data set. Overall, our findings suggest that both long distance dispersal and local retention are important sources of recruitment to populations of C. picta on LHI and that otolith chemistry of endemic species could be a useful benchmark for determining the prevalence of self‐recruitment in insular populations of other widespread species.     

Biocontrol: the response of native oystercatchers to a non‐native clam invasion

Global change, including invasive species introduction, has already had observable effects on migrant bird species, from northern breeding areas to wintering grounds. In this study we analyze the response of the Eurasian oystercatcher abundance to the density of an invasive clam species (Corbicula fluminea) and its potential role as biological control. As a case study, the oystercatcher population fluctuations over a 30‐yr time period, coupled with video‐recorded estimates of its feeding behavior on C. fluminea, and results from an exclosure experiment, were analyzed in the NW of the Iberian Peninsula. Results showed that oystercatchers exert a top‐down control over C. fluminea density. In addition, oystercatchers doubled its wintering numbers in a C. fluminea invaded estuary where they actively feed upon this invasive clam. Given that, the facilitative interaction between the invasive C. fluminea and the migratory Eurasian oystercatcher seems to respond to bottom‐up forces. Altogether, our results suggest that control measures applied to long term biological invasions must be carefully analyzed since non‐native species may be sustaining dependent native communities.     

Ecosystem engineering effects on species diversity across ecosystems: a meta‐analysis

Ecosystem engineering is increasingly recognized as a relevant ecological driver of diversity and community composition. Although engineering impacts on the biota can vary from negative to positive, and from trivial to enormous, patterns and causes of variation in the magnitude of engineering effects across ecosystems and engineer types remain largely unknown. To elucidate the above patterns, we conducted a meta‐analysis of 122 studies which explored effects of animal ecosystem engineers on species richness of other organisms in the community. The analysis revealed that the overall effect of ecosystem engineers on diversity is positive and corresponds to a 25% increase in species richness, indicating that ecosystem engineering is a facilitative process globally. Engineering effects were stronger in the tropics than at higher latitudes, likely because new or modified habitats provided by engineers in the tropics may help minimize competition and predation pressures on resident species. Within aquatic environments, engineering impacts were stronger in marine ecosystems (rocky shores) than in streams. In terrestrial ecosystems, engineers displayed stronger positive effects in arid environments (e.g. deserts). Ecosystem engineers that create new habitats or microhabitats had stronger effects than those that modify habitats or cause bioturbation. Invertebrate engineers and those with lower engineering persistence (<1 year) affected species richness more than vertebrate engineers which persisted for >1 year. Invertebrate species richness was particularly responsive to engineering impacts. This study is the first attempt to build an integrative framework of engineering effects on species diversity; it highlights the importance of considering latitude, habitat, engineering functional group, taxon and persistence of their effects in future theoretical and empirical studies.     

An invasive tree facilitates the persistence of native rodents on an over‐grazed floodplain in tropical Australia

In an ecosystem under simultaneous threat from multiple alien species, one invader may buffer the impact of another. Our surveys on a remote floodplain in the Kimberley region of north western Australia show that invasive chinee apple trees (Ziziphus mauritiana) provide critical refuge habitat for native rodents (pale field rats, Rattus tunneyi). Feral horses (Equus caballus) have trampled most of the remaining floodplain, but are excluded from the area around each chinee apple tree by thorny foliage. Although chinee apple trees constituted <10% of trees along our transects, they represented >50% of trees that harboured rat burrows. The mean number of burrows under each chinee apple tree was twice as high as under most other tree species, and we trapped more than seven times as many rats under chinee apple trees as under other types of trees. The extensive burrow systems under chinee apple trees contained female as well as male rats, whereas we only captured males around the smaller burrow systems under other tree species. Our data suggest that this invasive tree plays a critical role in the persistence of pale field rat populations in this degraded ecosystem, and that managers should maintain these trees (despite their alien origins) at least until feral horses have been removed.     

Ecosystem engineering by larvae of net-spinning stream caddisflies creates a habitat on the upper surface of stones for mayfly nymphs with a low resistance to flows

1. Field and laboratory experiments were conducted to examine the effect of larval retreats of the net‐spinning stream caddisfly Hydropsyche orientalis on abundances on flow exposed stone surfaces of nymphs of the mayfly Ephemerella setigera, which prefer slow flow conditions, and to determine whether the construction of retreats ameliorated the habitat and made it more suitable for E. setigera. 2. In a field experiment, artificial substrates with retreats of H. orientalis had higher E. setigera abundances than substrates lacking retreats. In addition, abundances of E. setigera nymphs increased significantly with those of H. orientalis larvae on the upper surface of boulders in streams. 3. The drift loss of E. setigera from plates, with and without retreats, was investigated along a current velocity gradient in a laboratory channel experiment. Nearly all E. setigera nymphs remained on the plates with retreats, even at the highest current velocity. In contrast, on the plates without retreats, the drift loss of E. setigera nymphs increased as the current velocity increased. 4. These results suggested that the habitat amelioration by H. orientalis retreats provided a refuge location for E. setigera nymphs and increased their abundances on stone surfaces exposed to flow forces.