Spatial variability in the abundance of pelagic invertebrate predators in relation to depth and turbidity

The abundance of pelagic invertebrate predators in relation to turbidity and depth gradients in Lake Hiidenvesi (southern Finland) were studied. In the shallow (<5 m) and the most turbid (up to 75 NTU) part of the lake, the community of invertebrate predators consisted of cyclopoid copepods (max biomass >500 μg dw l⁻¹) and Leptodora kindtiii (Focke) (17 μg dw l⁻¹), while in the less turbid (10–40 NTU) stratifying area Chaoborus flavicans (Meigen) dominated (max 146 μg dw l⁻¹). In the temporarily stratifying and moderately turbid basin Chaoborus and small-bodied invertebrate predators co-existed. Mysis relicta (Lovén) occurred only in the stratifying area (max 15 μg dw l⁻¹). The results suggested that both water depth and turbidity contributed to the community structure of Chaoborus flavicans. Depth great enough for stratification was of special importance and its effect was amplified by elevated turbidity, while high turbidity alone could not maintain chaoborid populations. Mysis relicta also requires a hypolimnetic refuge but is more sensitive to low oxygen concentrations and may therefore be forced to the epilimnion where it is vulnerable to fish predation. Cyclopoids as rapid swimmers can take advantage at elevated turbidity levels and coexist in high biomass with fish even in shallow water. Leptodora kindtii can form high biomass despite planktivorous fish providing that turbidity exceeds 20 NTU. The results demonstrated that depth and water turbidity can strongly regulate the abundance and species composition of invertebrate predators. These factors must thus be taken into account when applying food web management, which aims to reduce phytoplankton biomass by depressing planktivorous fish.     

Some allometric and non-allometric relationships between chlorophyll-a and abundance variables of phytoplankton

We analysed data from three Bulgarian reservoirs, with trophic status from meso to eutrophic. Two kinds of relations (non-allometric and allometric) of chlorophyll with phytoplankton density, biovolume and surface area were investigated. The non-allometric relationships compare these phytoplankton variables with chlorophyll-a concentration, while the allometric ones include comparisons of average individual volume (AIV) of phytoplankters with chlorophyll-a content per individual (Chl.N^–1), per unit biovolume (Chl.BV^–1) and per unit surface area (Chl.SA^–1).Maximum values of the rank correlation of the three non-allometric relationships were found in the eutrophic reservoir. The highest allometric correlation coefficients were observed in the mesotrophic reservoir. Two non-allometric relationships, Chl with N and Chl ith BV calculated on unified data from all three reservoirs showed lower significance and a non-linear character. Chl-SA relationship was always statistically significant and varied from linear to slightly non-linear when calculated on weighed values. Two allometric relationships, AIV with Chl.BV^–1 and AIV with Chl.N^–1 seem to be linear. A third AIV and Chl.SA^–1 was described by a polinomial of the second degree, indicating that the smallest and largest phytoplankton individuals have a similar chlorophyll content per unit surface area. At the highest trophy, the Chl.SA^–1 seemed lowest.The frequently investigated relationship between chlorophyll-a and biovolume ranged from statistically not significant in the mesotrophic to highly significant in the eutrophic reservoir. This tendency was generalized by obtaining a statistically significant rank correlation between the levels of significance of chlorophyll-biovolume correlations and the corresponding chlorophyll-a concentrations. The non-linear character of the chlorophyll-biovolume relationship over a wide range of trophy was probably caused by changes in surface area-biovolume ratio.Deceased.     

The feeding relationships of two invertebrate predators in a New Zealand river

The size frequency distributions and foods of the larvae of Archichauliodes diversus (Megaloptera: Corydalidae) and Stenoperla prasina (Plecoptera: Eustheniidae) were studied for a year in the Glentui River, South Island, New Zealand. These two species are the largest invertebrate predators inhabiting streams and rivers in New Zealand, where they are the only carnivorous members of their respective orders. Both species occupied the same habitat with A. diversus being slightly more abundant in most months. Many small larvae occurred within the sediments of the stream bed, whereas more larger larvae were found on stones lying on the surface. A wide size range of larvae was present throughout the year and the median size (in terms of head width) of both species was similar in most months. Larval growth could not be determined from field data and the life cycles of both species can be described as non-seasonal. Quantitative sampling in 5 months provided estimates of population densities. These were maximal in December when values of 136/m² for A. diversus and 114/m² for S. prasina were obtained. Larval Chironomidae and mayflies of the genus Deleatidium were the most frequently taken prey of both predators in all months, and no strong relationship between size or species of predator and size of prey was found. Caseless trichopteran larvae formed a less important component of the diets of both species and detritus was ingested by some individuals. No instances of cannibalism and only one example of cross-predation by each predator was seen. Diel sampling in November showed that large Deleatidium larvae were relatively more abundant in the guts of insect predators and in nocturnal drift samples than in the benthos. This suggests that their greater activity at night may increase their susceptibility to predation by nocturnal feeders. No clear ecological segregation of the two species with respect to habitat or prey utilization was found and there was no obvious interspecific competition for food, which appeared to be abundant at all times. Finally, the prevalence of non-seasonal life cycles in New Zealand aquatic insects is discussed in relation to the low degree of speciation in several groups.     

The distribution,abundance and seasonality of pelagic marine invertebrate larvae in the maritime Antarctic

A survey of pelagic larvae was undertaken between November 1992 and February 1995 at Signy Island, Antarctica (60° 43 minutes S, 45° 36 minutes W). A diver-towed net and hand-held plankton pump were used at five sites of varying depths (6 to 30 m) and benthic substrata, in a combination of monthly and fortnightly samples. Overall larval ecological diversity was much higher than expected, with 131 morphologically distinct larval forms collected, apparently representing most of the benthic phyla present. The species richness observed is comparable with levels recorded at temperate latitudes, and higher than Arctic data and the implications for Thorson''s rule (the inferred cline of reduced pelagic larval diversity towards high latitudes) is discussed. Larval abundances were low (mean 2.6 individuals per cubic metre) which were two to six orders of magnitude lower than peaks in comparable data from temperate and tropical zones. We suggest that the low abundances recorded are a reflection of both slow developmental rates and a high dilution of larvae, reducing synchrony and spreading larvae over larger distances. Three seasonal periods, during which different larval types occur, have been identified. Summer, late summer and winter spawning strategies were discernable, and in some groups larvae occurred throughout the year.     

The role of predators in driving warming-prey diversity relationships: An invertebrate perspective

Climate warming is one of the key driving forces of biodiversity loss. Yet, our understanding of underlying factors that link warming-biodiversity relationships at both local and regional spatial scales is limited. Here, I review how warming could change local-scale diversity of invertebrate animals. Specifically, I examine whether warming-prey diversity relationships are modulated by changes in predation at higher temperatures. I first review the predictions of bioenergetic models, and then carry out a systematic literature search to find empirical studies that have experimentally tested warming-prey diversity relationships together with warming-predation relationships as well as predation-prey diversity relationships both on land and in water. Empirical studies showed that warming consistently altered predation rates by either increasing or decreasing them. However, warming-prey diversity and predation-prey diversity relationships were inconsistent both on land and in water. Theoretical predictions of positive effects of warming on diversity in resource-rich environments were rarely tested by empirical studies. I suggest that warming-prey diversity and predation-prey diversity relationships can be better understood by incorporating three features of prey species: a) thermal tolerance, b) defense against predation, and c) ability to capture resources in warmer environments. I finally discuss the application of a prey trait-based conceptual framework to predict biodiversity changes from local to regional spatial scales in a warmer world.     

Skink and invertebrate abundance in relation to vegetation, rabbits and predators in a New Zealand dryland ecosystem

We explored the relationships between ground vegetation, ground fauna (native skinks and invertebrates), rabbits, and predators in a modified New Zealand dryland ecosystem. We hypothesised that vegetation cover would provide habitat for ground fauna. We also hypothesised that rabbits (Oryctolagus cuniculus) would reduce the abundance of these fauna by reducing vegetation, and by providing prey for mammalian predators (cats Felis catus and ferrets Mustela putorius) that consume ground fauna as secondary prey. We measured these variables at 30 sites across three pastoral properties in the South Island in 1996 and 2002. There were mostly positive relationships between vegetation ground cover and fauna captures in pitfall traps. Relatively few beetles and caterpillars were caught where cover was less than 80%, no millipedes were caught where cover was less than 70%, and few spiders and mostly no skinks, crickets, flies or slugs were caught where vegetation cover was less than 50%. Most grasshoppers were caught where cover ranged from 30 to 80%. Faunal species richness was also positively related to cover. This supports our hypothesis that ground vegetation provides habitat for skinks and invertebrates in this ecosystem. The introduction of rabbit haemorrhagic disease in 1997 provided a natural experiment to test the hypothesised indirect effects of rabbits on ground fauna. Declines in rabbits varied between properties, and vegetation cover and predator abundance changed according to the magnitude of these declines. However, skink and invertebrate abundance did not track these changes as expected, but instead varied more or less consistently between properties. Some fauna increased (skink captures quadrupled and cricket captures nearly doubled), others declined (flies, caterpillars and spiders), and some did not change (beetles, millipedes, slugs and grasshoppers, and faunal species richness and diversity). Therefore, rabbits, predators and vegetation did not affect changes in skinks and invertebrates in consistent ways. The dynamics of ground fauna are likely to be more influenced by factors other than those we measured.     

Incorporating invertebrate predators into theory regarding the timing of invertebrate drift

Theory concerning the timing of lotic invertebrate drift suggests that daytime-feeding fish cause invertebrates to restrict their drift behavior to the nighttime. However, there is growing evidence that the nighttime foraging of invertebrate predators also contributes to the nocturnal timing of drift, though it is unclear whether the nocturnal behavior of invertebrate predators is innate or proximately caused by fish. In two experiments, one conducted in a fish-bearing stream and a second in a fishless stream, we compared the drift patterns of Baetidae (Ephemeroptera) from channels with and without benthic invertebrate predators. We tested whether invertebrate predators affect the timing of drift, either as a proximate cause of nocturnal drift in the fishless stream (diel periodicity) or as a proximate cause of a pre-dawn peak in drift in the fish-bearing stream (nocturnal periodicity). In the fish-bearing stream experiment, a pre-dawn increase of baetid drift occurred independently of invertebrate predators, indicating that invertebrate predators were not the proximate cause of nocturnal periodicity in the stream. In the fishless stream experiment, invertebrate predators caused more baetid drift at night than during the day, indicating that invertebrate predators caused the nocturnal drift pattern we observed in the stream, and that invertebrate predators can influence drift timing independently of fish. Therefore, we suggest that both visually feeding fish and nocturnally foraging benthic predators, when present, affect the timing of invertebrate drift; visually feeding fish by reducing daytime drift, and benthic predators by increasing nighttime drift.     

Influence of submerged vegetation and fish abundance on water clarity in peri-urban eutrophic ponds

Despite the presence of high nutrient concentrations, most ponds located around Brussels (Belgium) show a considerable variation in turbidity. The importance of submerged macrophytes in maintaining the clear-water state requires identification of the main factors determining macrophyte abundance and diversity in ponds and small lakes. In this study, the inter-relationships between submerged macrophyte cover, fish abundance and turbidity were investigated in 13 eutrophic peri-urban ponds. Along a turbidity gradient, vegetation switched from dominance by Stoneworts (Chara and Nitella spp.) in the clearest ponds, to dominance by Potamogeton pectinatus in ponds with a slightly lower water transparency. Despite the presence of both P. pectinatus and Stoneworts in each of the vegetated ponds, only one became dominant. Only a very low abundance (around 20%) of submerged vegetation was found in ponds of intermediate turbidity, while macrophytes were absent in turbid ponds. Multi- and univariate analysis showed a marked difference in chemical, physical and biological properties between ponds deliberately used for fish stocking and ponds that were not. Macrophyte cover was significantly negatively correlated with turbidity and plankti-benthivorous fish abundance. No such correlation was observed with piscivorous fish abundance, except for pike that were associated with a charophyte vegetation in the study ponds. The strong relationship found between fish abundance and turbidity, its negative effect on submerged vegetation cover, and the importance of submerged vegetation in controlling phytoplankton abundance, should be taken into account when selecting ponds for fish stocking. It also suggests that the study ponds have a good potential for ecological quality restoration by biomanipulation.     

Pre-classification improves relationships between water clarity, light attenuation, and suspended particulates in turbid inland waters

Relationships between water clarity, light attenuation, and concentration of suspended particulates are important in water optics and remote sensing, but are not well described yet, especially for optically complex turbid inland waters. In this study, based on 3-year data from Chinese lakes (Lake Taihu, Lake Chaohu, and Three Gorges reservoir), we propose a new approach to describe the inter-relationships of these bio-optical variables. This approach includes a pre-classification step of the waters into three types based on a semi-analytical parameter C _s before establishing the relationships. Our results showed that the pre-classification of waters increased model accuracies both for Z _SD (Secchi depth) versus K _d (diffuse attenuation coefficient) and K _d versus TSM (total suspended matter concentration). The quasi-theoretical model described better the relationship between Z _SD and K _d than the empirical model. For the K _d versus TSM relationship, linear models proved suitable for the Type 2 and Type 3 waters, whereas the power function model gave a better fit for the Type 1 water. Testing of the proposed relations with an independent dataset showed mean absolute percentage errors (MAPE) mostly below 30%. The findings of this study clarify the relationships between Z _SD, K _d, and TSM, and improve our bio-optical understanding of complex turbid inland waters.     

Video analysis of predation by polyphagous invertebrate predators in the laboratory and field

This paper describes field and laboratory time-lapse video analyses of the behavioral responses of the groups: Arachnida: Acari, Araneae, and Opiliones; Myriapoda: Chilopoda; Hymenoptera: Formicidae; Crustacea: Isopoda; and Coleoptera: Staphylinidae to live eggs of the brown blowfly, Calliphora stygia F. (Diptera: Calliphoridae), used as factitious prey in two contrasting agricultural field margins and in the laboratory. Field video results showed that predation by mites was greatest in tree-lined boundaries while centipede numbers and activity were greater in post-and-wire boundaries. All except Staphylinidae showed clear diurnal patterns of activity and egg predation rate over the 12 h recording period. Based on the number of eggs removed, number of eggs examined, predator numbers, and predator activity, three indices were formulated that allowed predator groups to be ranked according to their effectiveness as predators. Commensal interactions between the mites and harvestmen, mediated via mite-pierced eggs, were suggested from field data and confirmed in the laboratory. Phalangium opilio preferred to feed on both manually and mite-pierced compared with untreated eggs, but showed a stronger preference for manually pierced ones than mite-pierced, consuming six times as many over the same period. This is the first demonstration of a commensal interaction between two agroecosystem predators. If commensalism is common in agroecosystems it could increase the effectiveness of biological control. It may also need to be incorporated within theoretical models and may complicate the extrapolation of laboratory-based feeding studies to field situations.     

Mutualistic relationships between phytoplankton and bacteria caused by carbon excretion from phytoplankton

For the competition system of phytoplankton and bacteria through inorganic phosphorus, our mathematical model showed that mutualistic relationships between them could occur due to production and consumption of extracellular organic carbon by phytoplankton and bacteria. In our model, phytoplankton are limited in their growth by light and phosphorus, and bacteria are limited in their growth by phosphorus and carbon released from phytoplankton. We adopted permanence as a criterion of the coexistence in mathematical analysis, and led necessary conditions of permanence in the model. Under these coexistence conditions, we estimated the strength of total effects of interactions between phytoplankton and bacteria at the steady state by press perturbation method. The results of this estimation indicated the mutualistic interactions between phytoplankton and bacteria. This suggests that mutualistic situation could occur due to the introduction of carbon flow from phytoplankton to bacteria, even if phytoplankton and bacteria compete with each other through common resource, inorganic phosphorus.     

Anurans as prey: an exploratory analysis and size relationships between predators and their prey

The vertebrate predators of post-metamorphic anurans were quantified and the predator–prey relationship was investigated by analysing the relative size of invertebrate predators and anurans. More than 100 vertebrate predators were identified (in more than 200 reports) and classified as opportunistic, convenience, temporary specialized and specialized predators. Invertebrate predators were classified as solitary non-venomous, venomous and social foragers according to 333 reviewed reports. Each of these categories of invertebrate predators was compared with the relative size of the anurans, showing an increase in the relative size of the prey when predators used special predatory tactics. The number of species and the number of families of anurans that were preyed upon did not vary with the size of the predator, suggesting that prey selection was not arbitrary and that energetic constraints must be involved in this choice. The relatively low predation pressure upon brachycephalids was related to the presence of some defensive strategies of its species. This compounding review can be used as the foundation for future advances in vertebrate predator–prey interactions.     

Long‐term patterns of invertebrate abundance and relationships to environmental factors in arid Australia

Resource pulses are a key feature of semi‐arid and arid ecosystems and are generally triggered by rainfall. While rainfall is an acknowledged driver of the abundance and distribution of larger animals, little is known about how invertebrate communities respond to rain events or to vegetative productivity. Here we investigate Ordinal‐level patterns and drivers of ground‐dwelling invertebrate abundance across 6 years of sampling in the Simpson Desert, central Australia. Between February 1999 and February 2005, a total of 174 381 invertebrates were sampled from 32 Orders. Ants were the most abundant taxon, comprising 83% of all invertebrates captured, while Collembola at 10.3% of total captures were a distant second over this period. Temporal patterns of the six invertebrate taxa specifically analysed (Acarina, ants, Araneae, Coleoptera, Collembola and Thysanura) were dynamic over the sampling period, and patterns of abundance were taxon‐specific. Analyses indicate that all six taxa showed a positive relationship with the cover of non‐Triodia vegetation. Other indicators of vegetative productivity (seeding and flowering) also showed positive relationships with certain taxa. Although the influence of rainfall was taxon‐dependent, no taxon was affected by short‐term rainfall (up to 18 days prior to survey). The abundance of Acarina, ants, and Coleoptera increased with greater long‐term rainfall (up to 18 months prior to survey), whilst Araneae showed the opposite effect. Temperature and dune zone (dune crest vs. swale) also had taxon‐specific effects. These results show that invertebrates in arid ecosystems are influenced by a variety of abiotic factors, at multiple scales, and that responses to rainfall are not as strong or as predictable as those seen for other taxa. Our results highlight the diversity of invertebrates in our study region and emphasize the need for targeted long‐term sampling to enhance our understanding of the ecology of these taxa and the role they play in arid ecosystems.     

Spatial avoidance of littoral and pelagic invertebrate predators by <Emphasis Type="Italic">Daphnia</Emphasis>

Studies on spatial avoidance behaviour of predators by prey often ignored the fact that prey typically face multiple predators which themselves interact and show a spatial pattern in abundance and predation rates (PRs). In a series of laboratory experiments, we investigated predation risk (PRI) and horizontal migration of the cladoceran Daphnia magna between open water and vegetation in response to two important invertebrate predators with a contrasting spatial distribution: pelagic Choaborus and vegetation-associated Ischnura. As expected, PRI by Chaoborus was higher in open water due to higher numbers and higher PRs of Chaoborus, while for Ischnura, PRI was highest in the vegetation due to higher densities, despite lower PRs of Ischnura. In accordance with this, Daphnia moved into the vegetation in the presence of the pelagic Chaoborus alone. In the presence of Ischnura alone, however, Daphnia showed no response. We hypothesize this may be the result of a constitutive behaviour of Daphnia to avoid pelagic fish, which impedes a response to the open water. In the combined predator treatment, Daphnia migrated to the open water zone. The increased risk of predation in the vegetation, due to a facilitating effect of Chaoborus on Ischnura PRs is believed to have caused this migration of the Daphnia. This response of Daphnia declined through time and Daphnia moved toward the vegetation. A decline in the activity of the Ischnura larvae through time may have switched the risk balance in favour of the vegetation environment.     

Non-lethal effects of invertebrate predators on Daphnia: morphological and life-history consequences of water mite kairomone

1. Here, we report morphological and life-historical changes in the cladoceran Daphnia ambigua in response to chemical cues released by the predatory water mite Piona chilensis . Both species are common inhabitants of southern temperate lakes.
2. We found significant differences in adult body size at first, second and third reproduction. Also, individuals exposed to kairomones had longer tail spines at first reproduction, and the resultant offspring had smaller bodies and shorter tail spines.
3. Exposure to mite cues did not exert effects on brood size at first reproduction, but decreased offspring number in subsequent broods. Similarly, only the second and third reproduction events were delayed by kairomone exposure.
4. The intrinsic population growth rate of predator-induced animals was lower than that in controls, but simulations based on a parameterized matrix model showed that the fitness costs could be overcome if the reported phenotypic responses reduced predation rate moderately. The gain in protection from predators needed to cancel out the reduction in fitness associated with predator cues was directly related to juvenile survival and fertility, and inversely related to adult survival.
5. This is the first work reporting phenotypic plasticity in Cladocera in response to kairomones released by water mites, which are conspicuous predators in many austral fresh waters.     

Centennial decline in North Sea water clarity causes strong delay in phytoplankton bloom timing

With climate warming, a widespread expectation is that events in spring, such as flowering, bird migrations, and insect bursts, will occur earlier because of increasing temperature. At high latitudes, increased ocean temperature is suggested to advance the spring phytoplankton bloom due to earlier stabilization of the water column. However, climate warming is also expected to cause browning in lakes and rivers due to increases in terrestrial greening, ultimately reducing water clarity in coastal areas where freshwater drain. In shallow areas, decreased retention of sediments on the seabed will add to this effect. Both browning and resuspension of sediments imply a reduction of the euphotic zone and Sverdrup's critical depth leading to a delay in the spring bloom, counteracting the effect of increasing temperature. Here, we provide evidence that such a transparency reduction has already taken place in both the deep and shallow areas of the North Sea during the 20th century. A sensitivity analysis using a water column model suggests that the reduced transparency might have caused up to 3 weeks delay in the spring bloom over the last century. This delay stands in contrast to the earlier bloom onset expected from global warming, thus highlighting the importance of including changing water transparency in analyses of phytoplankton phenology and primary production. This appears to be of particular relevance for coastal waters, where increased concentrations of absorbing and scattering substances (sediments, dissolved organic matter) have been suggested to lead to coastal darkening.     

Zooplankton community structure driven by vertebrate and invertebrate predators

Summary A zooplankton community was established in outdoor experimental ponds, into which a vertebrate predator (topmouth gudgeon: Pseudorasbora parva) and/or an invertebrate predator (phantom midge larva: Chaoborus flavicans) were introduced and their predation effects on the zooplankton community structure were evaluated. In the ponds which had Chaoborus but not fish, small- and medium-sized cladocerans and calanoid copepods were eliminated while rotifers became abundant. A large-sized cladoceran Daphnia longispina, whose juveniles had high helmets and long tailspines as anti-predator devices, escaped from Chaoborus predation and increased. In the ponds which had fish but not Chaoborus, the large-sized Daphnia was selectively predated by the fish while small-and medium-sized cladocerans and calanoid copepods predominated. In the ponds containing both Chaoborus and fish, the fish reduced the late instar larvae (III and IV) of Chaoborus but increased the early instar larvae (I and II). Small- and large-sized cladocerans were scarcely found. The former might have been eliminated by predation of the early instar larvae of Chaoborus, while the latter was probably predated by fish. Consequently, the medium-sized cladocerans, which may have succeeded in escaping from both types of predator, appeared abundantly. The results suggest that various combinations of vertebrate and invertebrate predators are able to drive various kinds of zooplankton community structure.     

Spatial relationships and mechanisms of coexistence between dominant and subordinate top predators

Most forest ecosystems contain a diverse community of top‐level predators. How these predator species interact, and how their interactions influence their spatial distribution is still poorly understood. Here we studied interactions among top predators in a guild of diurnal forest raptors in order to test the hypothesis that predation among competing predators (intraguild predation) significantly affects the spatial distribution of predator species, causing subordinate species to nest farther away from the dominant ones. The study analyzed a guild in southwestern Europe comprising three raptor species. For 8 years we studied the spatial distribution of used nests, breeding phenology, intraguild predation, territory occupancy, and nest‐builder species and subsequent nest‐user species. The subordinate species (sparrowhawk Accipiter nisus) nested farther away from the dominant species (goshawk A. gentilis), which preyed on sparrowhawks but not on buzzards Buteo buteo, and closer to buzzards, with which sparrowhawks do not share many common prey. This presumably reflects an effort to seek protection from goshawks. This potential positive effect of buzzards on sparrowhawks may be reciprocal, because buzzards benefit from old sparrowhawk nests, which buzzards used as a base for their nests, and from used sparrowhawk nests, from which buzzards stole prey. Buzzards occasionally occupied old goshawk nests. These results support our initial hypothesis that interspecific interactions within the raptor guild influence the spatial distribution of predator species in forest ecosystems, with intraguild predation as a key driver. We discuss several mechanisms that may promote the coexistence of subordinate and dominant predators and the spatial assembly of this raptor guild: spatial refuges, different breeding phenology, spatial avoidance, low territory occupancy between neighboring nesting territories, nest concealment and protection, and diet segregation.