Multi-species Aggregations Research Articles

Freshwater mussels prefer a diet of stramenopiles and fungi over bacteria

Freshwater mussels (Mollusca: Unionidae) play a crucial role in freshwater river environments where they live in multi-species aggregations and often serve as long-lived benthic ecosystem engineers. Many of these species are imperiled and it is imperative that we understand their basic needs to aid in the reestablishment and maintenance of mussel beds in rivers. In an effort to expand our knowledge of the diet of these organisms, five species of mussel were introduced into enclosed systems in two experiments. In the first, mussels were incubated in water from the Clinch River (Virginia, USA) and in the second, water from a manmade pond at the Commonwealth of Virginia’s Aquatic Wildlife Conservation Center in Marion, VA. Quantitative PCR and eDNA metabarcoding were used to determine which planktonic microbes were present before and after the introduction of mussels into each experimental system. It was found that all five species preferentially consumed microeukaryotes over bacteria. Most microeukaryotic taxa, including Stramenopiles and Chlorophytes were quickly consumed by all five mussel species. We also found that they consumed fungi but not as quickly as the microalgae, and that one species of mussel, Ortmanniana pectorosa, consumed bacteria but only after preferred food sources were depleted. Our results provide evidence that siphon feeding Unionid mussels can select preferred microbes from mixed plankton, and mussel species exhibit dietary niche differentiation.

Segregation and domain formation in non-local multi-species aggregation equations

A system of aggregation equations describing nonlocal interaction of two species is studied. When interspecies repulsive forces dominate intra-species repulsion, phase segregation may occur. This leads to the formation of distinct phase domains, separated by moving interfaces.The one dimensional interface problem is formulated variationally, and conditions for existence and nonexistence are established. The singular limit of large and short-ranged repulsion in two dimensions is then considered, leading to a two-phase free boundary problem describing the evolution of phase interfaces. Long term dynamics are investigated computationally, demonstrating coarsening phenomenon quantitatively different from classical models of phase separation. Finally, the interplay between long-range interspecies attraction and interfacial energy is illustrated, leading to pattern formation.

Niche specialization and community niche space increase with species richness in filter‐feeder assemblages

AbstractEcological theory posits that higher species richness should be associated with greater exploitation of resources and niche packing resulting from either increasing species niche overlap or specialization of species' niches. Research evaluating niche theory in animals tends to focus on organisms among functional feeding guilds, while resource partitioning might be more critical within functional groups. Freshwater mussels (Family: Unionidae) are a diverse and imperiled group of animals that are ideal models to test niche occupancy due to their functional similarity as filter‐feeders and their occurrence in spatially and temporally stable multispecies aggregations. We evaluated the relationship between species richness and the trophic niche area for 25 mussel species occurring in 22 aggregations in the southeastern United States using stable isotope analysis (δ13C and δ15N) of soft tissue (n = 1057). Mean species standard ellipse area decreased with species richness, whereas ellipse overlap was not related to richness, indicating increased niche specialization may be the primary mechanism allowing coexistence in species‐rich communities. Total community isotopic area increased with richness, suggesting species‐rich communities also use a broader range of resources and may not be species‐saturated. Overall, our data support the niche‐packing hypothesis by illustrating the importance of niche partitioning within a species‐rich guild of aquatic animals.

Commercial krill fishing within a foraging supergroup of fin whales in the Southern Ocean.

Commercial krill fishing within a foraging supergroup of fin whales in the Southern Ocean.

Observations of killer whales off East Antarctica, 82°-95°E, in 2009

Observations of killer whales (Orcinus orca) during a survey off East Antarctica, 82°–95°E revealed previously undescribed variations in pigmentation and group associations. During the survey 24 killer whale groups were sighted south of 60°S and classified, when possible, to Types A, B, or C based on their external morphology. Sufficient observation was available for nine groups to be classified: 2 groups of Type A; 1 mixed group of Type A and Type B; 3 groups of Type C; and 3 groups with eyepatch pigmentation intermediate in size between Types B and C. These whales may represent an intergrade between Types B and C or a previously unrecognised form. One of the ‘intermediate’ groups was observed feeding in a multi-species aggregation with other cetaceans in deep water. Clearly distinguishable Type A and Type B whales were observed feeding together in a mixed aggregation, the first time that this has been documented.

Review of potential line-transect methodologies for estimating abundance of dolphin stocks in the eastern tropical Pacific

A twelve-year hiatus in fishery-independent marine mammal surveys in the eastern tropical Pacific Ocean (ETP), combined with a mandate to monitor dolphin stock status under international agreements and the need for reliable stock status information to set dolphin bycatch limits in the tuna purse-seine fishery, has renewed debate about how best to assess and monitor ETP dolphin stock status. The high cost of replicating previous ship-based surveys has intensified this debate. In this review, transect methods for estimating animal abundance from dedicated research surveys are considered, with a focus on both contemporary and potential methods suitable for surveying large areas for dolphin species that can form large, multi-species aggregations. Covered in this review are potential improvements to the previous ship-based survey methodology, other ship-based methods, alternative approaches based on high-resolution imagery and passive acoustics, and combinations of ship-based and alternative approaches. It is concluded that for immediate management needs, ship-based surveys, with some suggested modifications to improve precision, are the only reliable option despite their high cost. However, it is recommended that a top research priority should be development of composite methods. Pilot studies on the use of high-resolution imagery and passive acoustics for development of indices of relative abundance to be used in composite methods should be part of any future ship-based survey efforts.

Interspecific interactions among three species of sea turtle using a common resting area.

Interspecific interactions among three species of sea turtle using a common resting area.

Intra- and interspecific competition resulting from spatial coexistence among larvae of closely-related caddisflies from the genus Hydropsyche.

Caddisfly larvae commonly inhabit freshwater ecosystems, where they often create multi-species aggregations. However, while several strategies have been developed to avoid or reduce inter- and intraspecific interactions, most species choose the same time to seek a suitable place for pupation, which can increase competition. The current study assesses the competitive interactions among larvae (5th instar) of three co-existing Hydropsyche species, viz. H. contubernalis, H. pellucidula, and H. modesta, analysing their direct one-on-one interaction and various morphological features, such as size, weight, and mandibles. More than half of the interspecific conflicts ended with a draw, and 80% of intraspecific interactions with a decisive outcome. In fights between species, H. pellucidula was the most successful, and H. modesta the weakest. Our results confirm that among the larvae, competitive interactions were usually decided by body size, especially that of the head capsule. Although wider head capsule and higher weight were advantageous for ~60% of winning larvae, there were no distinct winning species. The chewing mouthpart turned out to be supportive in the fight: regardless of the species, longer and wider mandibles were significant for winning specimens, but not the distance between mandibles. Hence, acquiring a suitable place for pupation is determined by the possession of certain features enhancing the fighting potential of individual larvae, which does not exclude any species from the possibility of closing the life cycle. Future studies on interactions among caddisfly larvae could include experience in fights, volitional features and stridulation (not tested).

A History of the Tuna-Dolphin Problem: Successes, Failures, and Lessons Learned

Multispecies aggregations of tuna, dolphins, and seabirds are prevalent and conspicuous in the vast waters of the eastern tropical Pacific and form the basis of a commercial fishery for yellowfin tuna (Thunnus albacares) through setting on schools of dolphins, which is among the largest tuna fisheries in the world. Incidental dolphin mortality associated with the development and early years of the fishery was high; by 1993 it was estimated that eastern spinner dolphins (Stenella longirostris orientalis) had been reduced to 44% and northeastern offshore spotted dolphins (S. attenuata attenuata) to 19% of pre-fishery levels. Efforts to reduce this mortality began at the inception of the fishery and comprised a diverse array of approaches: modifications to fishing methods and fishing gear (backdown, Medina panel, high-intensity floodlights, swimmers to disentangle and release dolphins); U.S. legislation (through the U.S. Marine Mammal Protection Act, MMPA, and subsequent amendments); international agreements (including the International Dolphin Conservation Program that established dolphin mortality limits, and the legally binding multilateral Agreement on the International Dolphin Conservation Program); and economic incentives [notably through establishment of the U.S. dolphin-safe label and positive certification by the Marine Stewardship Council (MSC)]. Together, these bycatch mitigation efforts have been remarkably successful; dolphin mortality due to entanglement as recorded by fisheries observers (hereafter, entanglement mortality) has been reduced by > 99%. Despite this, the degree to which dolphin populations have recovered remains unclear. Multiple lines of evidence indicate that individual dolphins experience multiple sets in their lifetimes and although causality has not been established, research suggests that chase and encirclement might have impacts on dolphins in addition to entanglement mortality. These impacts potentially include increased fetal and/or calf mortality, separation of nursing females and their calves, decreased fecundity, increased predation, disruption of mating and other social systems, and ecological disruption. The strong management emphasis on monitoring entanglement mortality, and the infrastructure necessary to support this monitoring (in particular, 100% observer coverage on large purse-seiners) require funding to the extent that other activities, particularly continued surveys to monitor stock status and clarify the potential influence of other effects of the fishery on dolphin populations, are currently inadequately funded.

Population dynamics of microbial cross-feeding are determined by co-localization probabilities and cooperation-independent cheater growth

As natural selection acts on individual organisms the evolution of costly cooperation between microorganisms is an intriguing phenomenon. Introduction of spatial structure to privatize exchanged molecules can explain the evolution of cooperation. However, in many natural systems cells can also grow to low cell concentrations in the absence of these exchanged molecules, thus showing “cooperation-independent background growth”. We here serially propagated a synthetic cross-feeding consortium of lactococci in the droplets of a water-in-oil emulsion, essentially mimicking group selection with varying founder population sizes. The results show that when the growth of cheaters completely depends on cooperators, cooperators outcompete cheaters. However, cheaters outcompete cooperators when they can independently grow to only ten percent of the consortium carrying capacity. This result is the consequence of a probabilistic effect, as low founder population sizes in droplets decrease the frequency of cooperator co-localization. Cooperator-enrichment can be recovered by increasing the founder population size in droplets to intermediate values. Together with mathematical modelling our results suggest that co-localization probabilities in a spatially structured environment leave a small window of opportunity for the evolution of cooperation between organisms that do not benefit from their cooperative trait when in isolation or form multispecies aggregates.

Variation in Species Composition, Size and Fitness of Two Multi-Species Sea Turtle Assemblages Using Different Neritic Habitats

The neritic environment is rich in resources and as such plays a crucial role as foraging habitat for multi-species marine assemblages, including sea turtles. However, this habitat also experiences a wide array of anthropogenic threats. To prioritize conservation funds, targeting areas that support multi-species assemblages is ideal. This is particularly important in the Gulf of Mexico where restoration actions are currently ongoing following the Deepwater Horizon oil spill. To better understand these areas in the Gulf of Mexico, we characterized two multi-species aggregations of sea turtles captured in different neritic habitats. We described species composition and size classes of turtles, and calculated body condition index for 642 individuals of three species captured from 2011 to 2019: 13.6% loggerheads (Caretta caretta), 44.9% Kemp’s ridleys (Lepidochelys kempii) and 41.4% green turtles (Chelonia mydas). Species composition differed between the two sites with more loggerheads captured in seagrass and a greater proportion of green turtles captured in sand bottom. Turtles in sand bottom were smaller and weighed less than those captured in seagrass. Although small and large turtles were captured at both sites, the proportions differed between sites. Body condition index of green turtles was lower in sand habitat than seagrass habitat; there was no difference for Kemp’s ridleys or loggerheads. In general, smaller green turtles had a higher body condition index than larger green turtles. We have identified another habitat type used by juvenile sea turtle species in the northern Gulf of Mexico. In addition, we highlight the importance of habitat selection by immature turtles recruiting from the oceanic to the neritic environment, particularly for green turtles.

A game of alignment: Collective behavior of multi-species

We study the (hydro-)dynamics of multi-species driven by alignment. What distinguishes the different species is the protocol of their interaction with the rest of the crowd: the collective motion is described by different communication kernels, ϕαβ, between the crowds in species α and β. We show that flocking of the overall crowd emerges provided the communication array between species forms a connected graph. In particular, the crowd within each species need not interact with its own kind, i.e., ϕαα=0; different species which are engaged in such ‘game’ of alignment require a connecting path for propagation of information which will lead to the flocking of overall crowd. The same methodology applies to multi-species aggregation dynamics governed by first-order alignment: connectivity implies concentration around an emerging consensus.

Drifting along in the open-ocean: The associative behaviour of oceanic triggerfish and rainbow runner with floating objects

Multispecies aggregations at floating objects are a common feature throughout the world's tropical and subtropical oceans. The evolutionary benefits driving this associative behaviour of pelagic fish remains unclear and information on the associative behaviour of non-tuna species remains scarce. This study investigated the associative behaviour of oceanic triggerfish (Canthidermis maculata) and rainbow runner (Elagatis bipinnulata), two major bycatch species in the tropical tuna purse seine fishery, at floating objects in the western Indian Ocean. A total of 24 rainbow runner and 46 oceanic triggerfish were tagged with acoustic transmitters at nine drifting FADs equipped with satellite linked receivers. Both species remained associated with the same floating object for extended periods; Kaplan-Meier survival estimates (considering the censored residence time due to equipment failure and fishing) suggested that mean residence time by rainbow runner and oceanic triggerfish was of 94 and 65 days, respectively. During daytime, the two species increased their home range as they typically performed short excursions (<2 h) away from the floating objects. Rainbow runner performed more excursions per unit time than oceanic triggerfish; the mean excursion index was 0.86 (±0.8 SD) for oceanic triggerfish and 1.31 (±1.1 SD) for rainbow runner. Ambient light intensity appears to be the stimulus triggering the onset and end of the associative modes. The observed prolonged residency of these two major bycatch species suggests that they are more vulnerable to the tropical tuna purse seine gear than the targeted tuna species.

Behavioral and chemical antipredator mechanisms in ground beetles: an attempt to reconcile within a phylogenetic frame

Like other coleopterans, Carabids are recognized for the use of passive and active strategies against their enemies. They are known to produce dangerous and distasteful chemicals and to use anti-predator behaviors such crypsis/mimicry, gregariousness, intra- and interspecific helpful interactions, sound production and aposematism. While defensive chemicals have been an important element in the successful diversification of ground beetles, in many tribes of this wide adephagan family many other systems have evolved and discovered. Here we present a review on the current knowledge of the avoidance mechanisms in carabids, with a discussion of data on chemical products, morphological adaptations and behaviors used against vertebrate and invertebrate predators. The most widespread strategy is discouragement of the predators using pygidial gland secretions, but passive anti-predator strategies are also displayed as group-protecting behavior through intraspecific aggregations or communal roosting. Most adult carabids tend to be dark in color and thus less detectable, but chemically well-protected taxa use the opposite strategy, displaying bright colors related to mimicry or aposematism. In aposematic species, group-protecting behavior has probably evolved from intraspecific gregariousness into multispecies aggregations. Larval behavioral strategies are related more closely to the epigean or underground lifestyle. In surface-living larvae, cannibalism avoidance and the usage of defensive substances have been reported for Chlaeniini. In this tribe we found an interesting coincidence between a high level of toxicity/distastefulness and a complex larval behavior. Based mainly on the genus-level supertree of Beutel et al. (2008) and the phylogenetic analyses of Ober &amp;amp; Maddison (2008) we reconstructed the evolutionary relationships among the chemical classes isolated inside the tribes. The scenario shows that several semiochemical classes (quinone/benzoquinones, formic acid, m-cresol, methacrylic acid, isovaleric acid, ß-necrodol, benzaldehyde, etc.) found in carabids are at least in part related to their life style and habitat selection. The proposed relationship still lacks other chemical data of the missing genera/species and even if the knowledge of carabid anti-predator strategies still seems to be in the pioneer stage, future studies on carabid anti-predator behavior look very promising.

Virome heterogeneity and connectivity in waterfowl and shorebird communities

Models of host-microbe dynamics typically assume a single-host population infected by a single pathogen. In reality, many hosts form multi-species aggregations and may be infected with an assemblage of pathogens. We used a meta-transcriptomic approach to characterize the viromes of nine avian species in the Anseriformes (ducks) and Charadriiformes (shorebirds). This revealed the presence of 27 viral species, of which 24 were novel, including double-stranded RNA viruses (Picobirnaviridae and Reoviridae), single-stranded RNA viruses (Astroviridae, Caliciviridae, Picornaviridae), a retro-transcribing DNA virus (Hepadnaviridae), and a single-stranded DNA virus (Parvoviridae). These viruses comprise multi-host generalist viruses and those that are host-specific, indicative of both virome connectivity (host sharing) and heterogeneity (host specificity). Virome connectivity was apparent in two well described multi-host virus species -avian coronavirus and influenza A virus- and a novel Rotavirus species that were shared among some Anseriform species, while virome heterogeneity was reflected in the absence of viruses shared between Anseriformes and Charadriiformes, as well as differences in viral abundance and alpha diversity among species. Overall, we demonstrate complex virome structures across host species that co-exist in multi-species aggregations.

Molecular phylogeny, ecology and multispecies aggregation behaviour of bombardier beetles in Arizona.

Aggregations of conspecific animals are common and have been documented in most phyla. Multispecies aggregations are less common and less well studied. Eight species of Brachinus beetles —famous for their unique, highly effective, chemical defense—regularly settle together form large diurnal multispecies aggregations in dark, moist areas in riparian habitats in the Sonoran Desert Region. Here, we document these multispecies aggregations and investigate the incidence and dynamics of aggregation behavior. Analysis of species composition of 59 field-collected aggregations revealed that 71% contained more than one species, eight species regularly co-occurred in aggregations, and no two species showed a preference to aggregate with one another. We provide the first phylogenetic analyses of participants in multispecies aggregations, and find that Brachinus species found together in aggregations are not each other’s closest relatives but rather are dispersed throughout the phylogeny of the genus. Further, we find no tendency for species to aggregate with close relatives more frequently than distant relatives. Laboratory experiments on B. elongatulus showed that it chose to settle in occupied shelters over empty shelters. Experiments with B. hirsutus and B. elongatulus showed that B. hirsutus prefers to settle under shelters housing heterospecifics over conspecifics. Our findings suggest that these multispecies aggregations do not form by chance, but rather are initiated by a genus-wide aggregation cue associated with the presence of individuals already in a shelter, which is likely to be chemical and potentially tactile in nature.

Bacterial Associates of a Gregarious Riparian Beetle With Explosive Defensive Chemistry.

Bombardier beetles (Carabidae: Brachininae) are well known for their unique explosive defensive chemistry. These beetles are found in riparian corridors throughout the American Southwest, where they commonly form large diurnal multispecies aggregations in moist areas under rocks, in crevices, and in leaf litter. Using high throughput 16S amplicon sequencing, we provide the first microbiome survey of a bombardier beetle, Brachinus elongatulus, collected from two sites in Arizona. Two bacterial taxa were present in all individuals sampled: Enterococcus and Dysgonomonas. Enterococcus has been implicated in the production of fecal aggregation pheromone components, which have been shown to regulate aggregation in the German cockroach; it is possible that Enterococcus plays a similar role in Brachinus. Dysgonomonas was found in all the secretory cells of the defensive system and gut samples. Additional studies are needed to determine if these microbes play a role in these beetles’ unique chemical defense. Results also show that the majority of B. elongatulus individuals collected from both sites were infected with Spiroplasma. Many Spiroplasma are intracellular, vertically transmitted insect symbionts that may manipulate host reproduction (e.g., cause male-killing) or provide resistance to nematodes and/or parasitoid wasps. Defensive protection could be especially beneficial to B. elongatulus, which are frequently parasitized by horsehair worms (Nematomorpha). In sum, findings suggest several testable hypotheses on the effects bacteria may have on bombardier beetle behavior and physiology.

Multi-species consumer jams and the fall of guarded corals to crown-of-thorns seastar outbreaks.

Outbreaks of predatory crown-of-thorns seastars (COTS) can devastate coral reef ecosystems, yet some corals possess mutualistic guardian crabs that defend against COTS attacks. However, guarded corals do not always survive COTS outbreaks, with the ecological mechanisms sealing the fate of these corals during COTS infestations remaining unknown. In August 2008 in Moorea (17.539° S, 149.830° W), French Polynesia, an unusually dense multi-species aggregation of predators was observed feeding upon guarded corals following widespread coral decline due to COTS predation. Concurrent assaults from these amplified, mixed-species predator guilds likely overwhelm mutualistic crab defense, ultimately leading to the fall of guarded corals. Our observations indicate that guarded corals can sustain devastating COTS attacks for an extended duration, but eventually concede to intensifying assaults from diverse predators that aggregate in high numbers as alternative prey decays. The fall of guarded corals is therefore suggested to be ultimately driven by an indirect trophic cascade that leads to amplified attacks from diverse starving predators following prey decline, rather than COTS assaults alone.

Multi-species consumer jams and the fall of guarded corals to crown-of-thorns seastar outbreaks

Outbreaks of predatory crown-of-thorns seastars (COTS) can devastate coral reef ecosystems, yet some corals possess mutualistic guardian crabs that defend against COTS attacks. However, guarded corals do not always survive COTS outbreaks, with the ecological mechanisms sealing the fate of these corals during COTS infestations remaining unknown. In August 2008 in Moorea (17.539° S, 149.830° W), French Polynesia, an unusually dense multi-species aggregation of predators was observed feeding upon guarded corals following widespread coral decline due to COTS predation. Concurrent assaults from these amplified, mixed-species predator guilds likely overwhelm mutualistic crab defense, ultimately leading to the fall of guarded corals. Our observations indicate that guarded corals can sustain devastating COTS attacks for an extended duration, but eventually concede to intensifying assaults from diverse predators that aggregate in high numbers as alternative prey decays. The fall of guarded corals is therefore suggested to be ultimately driven by an indirect trophic cascade that leads to amplified attacks from diverse starving predators following prey decline, rather than COTS assaults alone.

Multi-species consumer jams and the fall of guarded corals to crown-of-thorns seastar outbreaks

Outbreaks of predatory crown-of-thorns seastars (COTS) can devastate coral reef ecosystems, yet some corals possess mutualistic guardian crabs that defend against COTS attacks. However, guarded corals do not always survive COTS outbreaks, with the ecological mechanisms sealing the fate of these corals during COTS infestations remaining unknown. In August 2008 in Moorea (17.539° S, 149.830° W), French Polynesia, an unusually dense multi-species aggregation of predators was observed feeding upon guarded corals following widespread coral decline due to COTS predation. Concurrent assaults from these amplified, mixed-species predator guilds likely overwhelm mutualistic crab defense, ultimately leading to the fall of guarded corals. Our observations indicate that guarded corals can sustain devastating COTS attacks for an extended duration, but eventually concede to intensifying assaults from diverse predators that aggregate in high numbers as alternative prey decays. The fall of guarded corals is therefore suggested to be ultimately driven by an indirect trophic cascade that leads to amplified attacks from diverse starving predators following prey decline, rather than COTS assaults alone.