Black-fronted Titi Monkeys Research Articles

Social Interactions in Wild Black-Fronted Titi Monkeys (Callicebus nigrifrons)

Social Interactions in Wild Black-Fronted Titi Monkeys (Callicebus nigrifrons)

Impact of predator model presentation paradigms on titi monkey alarm sequences

Predator presentation experiments are widely used to investigate animal alarm vocalizations. They usually involve presentations of predator models or playbacks of predator calls, but it remains unclear whether the two paradigms provide similar results, a major limitation when investigating animal syntactic and semantic capacities. Here, we investigate whether visual and acoustic predator cues elicit different vocal reactions in black-fronted titi monkeys (Callicebus nigrifrons). We exposed six groups of wild titi monkeys to visual models or playbacks of vocalizations of raptor or felid. We characterized each group’s vocal reactions using sequence parameters known to reliably encode predatory events in this species. We found that titi monkeys’ vocal reactions varied with the predator species but also with the experimental paradigm: while vocal reactions to raptor vocalizations and models were similar, felid vocalizations elicited heterogeneous, different reactions from that given to felid models. We argue that subjects are not familiar with felid vocalizations, because of a lack of learning opportunities due to the silent behaviour of felids. We discuss the implication of these findings for the semantic capacities of titi monkeys. We finally recommend that playbacks of predator vocalizations should not be used in isolation but in combination with visual model presentations, to allow fine-grained analyses of the communication system of prey species.Significance statementIt is common to present prey species with predator models or predator calls to study their vocal reactions. The two paradigms are often used independently, but it remains unclear whether they provide similar results. Here, we studied the vocal reactions of titi monkeys to calls and models of raptors and felids. We show that titi monkeys seem to recognize the vocalizations of raptors but not those of felids. The study of the vocal reactions emitted when titi monkeys cannot clearly identify the threat allows us to draw accurate hypotheses about the meaning of titi monkeys’ alarm utterances. We argue that playbacks of predator calls should be used in conjunction with model presentations, which can allow us to better investigate the information and the structure of the alarm systems.

Animal linguistics in the making: the Urgency Principle and titi monkeys’ alarm system

The emergent field of animal linguistics applies linguistics tools to animal data in order to investigate potential linguistic-like properties of their communication. One of these tools is the “Urgency Principle”, a pragmatic principle stating that in an alarm sequence, calls providing information about the nature or location of a threat must come before those that do not. This theoretical principle has helped understand the alarm system of putty-nosed monkeys, but whether it is relevant for animal communication systems more generally remains to be tested. Moreover, while animal communication systems can convey information via a large set of encoding mechanisms, the Urgency Principle was developed for only one encoding mechanism, call ordering. Here, we propose to extend this principle to other encoding mechanisms and empirically test this with the alarm call system of black-fronted titi monkeys (Callicebus nigrifrons). We investigated how information about the context of emission unfolded with the emission of successive calls. Specifically, we analysed how contextual parameters influenced the gradual sequential organization of the first 50 calls in the sequence, using methods borrowed from computational linguistics and random forest algorithms. We hypothesized that, if the extended Urgency Principle reflected the sequential organization of titi monkey alarm call sequences, mechanisms encoding urgent information about the predatory situation should appear before encoding mechanisms that do not. Results supported the hypothesis that mechanisms encoding for urgent information relating to a predator event consistently appeared before mechanisms encoding for less-urgent social information. Our study suggests that the extended Urgency Principle applies more generally to animal communication, demonstrating that conceptual tools from linguistics can successfully be used to study nonhuman communication systems.

Dramatic decline in a titi monkey population after the 2016-2018 sylvatic yellow fever outbreak in Brazil.

Platyrrhini are highly vulnerable to the yellow fever (YF) virus. From 2016 to 2018, the Atlantic Forest of southeast Brazil faced its worst sylvatic YF outbreak in about a century, thought to have killed thousands of primates. It is essential to assess the impact of this epidemic on threatened primate assemblages to design effective conservation strategies. In this study, we assessed the impact of the 2016-2018 YF outbreak on a geographically isolated population of Near Threatened black-fronted titi monkeys (Callicebus nigrifrons) in two Atlantic Forest patches of the Santuário do Caraça, MG, Brazil. Extensive preoutbreak monitoring, conducted between 2008 and 2016, revealed that the home range and group sizes of the population remained stable. In 2016, the population size was estimated at 53-57 individuals in 11-12 groups. We conducted monitoring and playback surveys in 2019 and found that the population had decreased by 68% in one forest patch and completely vanished in the other, resulting in a combined decline of 80%. We discuss this severe loss of a previously stable population and conclude that it was highly likely caused by the YF outbreak. The remaining population is at risk of disappearing completely because of its small size and geographic isolation. A systematic population surveys of C. nigrifrons, along other sensible Platyrrhini species, is needed to re-evaluate their current conservation status.

Mammals in atlantic forest remnants of Barbacena, Minas Gerais

Abstract Habitat loss and fragmentation are the main causes of biodiversity decline, since changes in environmental and ecological conditions directly affect species richness, abundance, and distribution. This study aimed to identify medium- and large-sized mammals occurring in three Atlantic Forest remnants located in the Barbacena campus of the Federal Institute of Southeast Minas Gerais (IFSudesteMG). The species were recorded in track plots and through active search for direct and indirect signs. 16 species distributed in six orders and 14 families were identified, including some vulnerable and threatened species such as Lycalopex vetulus (meadow fox), Lontra longicaudis (otter), and Callicebus nigrifrons (black-fronted titi monkey). Canis familiaris (domestic dog) and Didelphis sp. (opossum) were the species most frequently observed in the track plots. The largest fragment had the greatest species richness, with 15 species, or 93.75% of the total. The number of species shared among the three sampled areas was 31.2%. The similarities identified between the fragments indicate the need for higher connectivity among them, through the creation of ecological corridors to allow the movement and, consequently, gene flux among the populations, favoring the maintenance of important ecosystem services in the region. Although small, the study area plays a major role in mammal conservation in the region, preserving species from the Cerrado and the Atlantic Forest domains. To reduce potential impacts on the local fauna, management and conservation efforts should be put forward.

From dropping to dropping: The contribution of a small primate to seed dispersal in Atlantic Forest

The dynamic interaction between animals and plants through frugivory and seed dispersal is one of several ecological processes that modulates tropical biodiversity. Here we evaluated the potential role of a highly-frugivorous Neotropical primate, the black-fronted titi monkey (Callicebus nigrifrons), as seed disperser. We studied two titi monkey groups in semideciduous Atlantic Forest remnants. Each group fed on over 49 zoochorous plant species in about one year and ingested seeds from nearly a half of them, especially those with small seeds (<0.5 cm). The groups of titi monkeys defecated a large number of seeds, reaching over 300 seeds per day (1–305). More than half of the total deposited seeds and seed species germinated after gut passage, however gut passage reduced germination success in three of five evaluated species. Feces were deposited in small clumps distributed across groups’ home range. We suggest that the observed distribution pattern of feces may enhance plant reproductive fitness by increasing the probability of seeds being deposited far from parent plants, in novel and favorable sites. We concluded that the seed handling and deposition behavior of black-fronted titi monkey make this primate an important agent for Atlantic forest regeneration.

A new species of Amblyomma (Acari: Ixodidae) associated with monkeys and passerines of the Atlantic rainforest biome, Southeastern Brazil

Recent studies have reported several larvae of an unidentified Amblyomma species on passerine birds in Atlantic rainforest fragments in southeastern Brazil. These larvae yielded a unique 16S rRNA haplotype designated as Amblyomma sp. haplotype Nazaré, which showed nucleotide identity levels of 91% to Amblyomma parkeri Fonseca & Aragão, 1952 and 88% to Amblyomma longirostre (Koch, 1844). Herein, we describe Amblyomma sp. haplotype Nazaré as a new species, Amblyomma romarioi n. sp. Martins, Luz & Labruna, through a formal description of the male and female adult stages. Amblyomma romarioi is morphologically and genetically most closely related to A. parkeri, A. longirostre and Amblyomma geayi Neumann, 1899. Among males, the rectangular basis capituli and rounded coxa I spurs separates A. romarioi from A. parkeri, A. longirostre, and A. geayi, which have basis capituli triangular or slightly hexagonal, and pointed coxa I spurs. Among females, the V-shaped genital aperture and coxa I rounded spurs of A. romarioi contrasts to the U-shaped genital aperture and coxa I pointed spurs in A. parkeri, A. longirostre, and A. geayi. Larvae of A. romarioi have been collected on 24 species of passerines. The few records of nymphs and adults were on the black-fronted titi monkey Callicebus nigrifrons (Spix, 1823). The current distribution of A. romarioi is restricted to the Brazilian Atlantic rainforest, southeastern Brazil, in areas with altitude between 363 and 1600 m, within the distribution of C. nigrifrons. We discuss ecological features of Amblyomma romarioi, comparatively to A. parkeri, A. longirostre and A. geayi. The present study increases the Brazilian tick fauna to 74 species.

Active anti-predator behaviour of red titi monkeys (Plecturocebus cupreus).

Due to their inconspicuous behaviour and colouration, it has been assumed that titi monkeys' main anti-predator behaviour is passive crypsis and hiding. So far, active predator mobbing has been documented only for black-fronted titi monkeys, Callicebus nigrifrons. Here we report for the first time mobbing behaviour of red titi monkeys, Plecturocebus cupreus (previously Callicebus cupreus), as reaction to an ocelot (Leopardus pardalis) and a Boa constrictor. We also report other active anti-predator behaviours, such as alarm calling and approaching, as reactions to tayras (Eira barbara) and raptors. Our observations provide additional evidence for sex differences in anti-predator behaviour, possibly related to the evolution and maintenance of social monogamy.

Contextual encoding in titi monkey alarm call sequences

Many primates produce one type of alarm call to a broad range of events, usually terrestrial predators and non-predatory situations, which raises questions about whether primate alarm calls should be considered ‘functionally referential’. A recent example is black-fronted titi monkeys, Callicebus nigrifrons, which emit sequences of B-calls to terrestrial predators or when moving towards or near the ground. In this study, we reassess the context specificity of these utterances, focussing both on their acoustic and sequential structure. We found that B-calls could be differentiated into context-specific acoustic variants (terrestrial predators vs. ground-related movements) and that call sequences to predators had a more regular sequential structure than ground-related sequences. Overall, these findings suggest that the acoustic and temporal structure of titi monkey call sequences discriminate between predator and non-predatory events, fulfilling the production criterion of functional reference. Primate terrestrial alarm calls are at the centre of an ongoing debate about meaning in animal signals. Primates regularly emit one alarm call type to ground predators but often also to various non-predatory events, raising questions about the referential nature of these signals. In this study, we report observational and experimental data from wild titi monkeys and show that terrestrial alarm calls are usually given in sequences of acoustically distinct variants composed in structurally distinct ways depending on the external event. These differences are salient and could help recipients to distinguish the nature of the call eliciting event. Since most previous studies on animal alarm calls have not checked for acoustic variants within different call classes, it may be premature to conclude that primate terrestrial calls do not meet the criteria of functional reference.

Mining noise affects loud call structures and emission patterns of wild black-fronted titi monkeys.

Anthropogenic noise pollution is increasing and can constrain acoustic communication in animals. Our aim was to investigate if the acoustic parameters of loud calls and their diurnal pattern in the black-fronted titi monkey (Callicebus nigrifrons) are affected by noise produced by mining activity in a fragment of Atlantic Forest in Brazil. We installed two passive acoustic monitoring devices to record sound 24h/day, 7days every 2months, for a year; one unit was close to an opencast mine and the other 2.5km away from it. Both sites presented similar habitat structures and were inhabited by groups of black-fronted titi monkeys. We quantified the noise at both sites by measuring the equivalent continuous sound level every 2 months for 1 year and quantified the emission of loud calls by titi monkeys through visual inspection of the recordings. The close site presented higher ambient noise levels than the far site. The quantitative comparison of loud calls of black-fronted titi monkeys between the two sites showed less calling activity in the site close to the mine than in the site further away. Approximately 20% of the calls detected at the site close to the mine were masked by noise from truck traffic. Loud calls were longer at the site far from the mine and the diurnal patterns of vocal activity differed in the amount of calling as well as in the timing of peak calling activity between the two sites. Our results indicate that mining noise may constrain titi monkeys' long-distance vocal communication. Loud calls occupy a similar frequency band to mining noise, and an increase in ambient noise may be triggering black-fronted titi monkeys to adjust their long-distance communication patterns to avoid masking of their calls. Given that vocalizations are an important means of social interaction in this species, there are concerns about the impact of mining noise on populations exposed to this human activity.

Sleeping above the enemy: Sleeping site choice by black‐fronted titi monkeys (Callicebus nigrifrons)

The costs imposed by predation may result in behavioral adaptations to reduce mortality risk, including the choice and use of sleeping sites. The threat of predation, however, is rarely the sole force shaping sleeping site choice, which is likely to reflect other factors such as foraging needs as well. Here we describe the use of sleeping sites by three groups of small Neotropical monkeys, the black-fronted titi monkeys (Callicebus nigrifrons), and evaluate the role of predation pressure and foraging optimization in their choice of sleeping sites. We monitored each group for 9-20 months at two Atlantic Forest sites in southeastern Brazil. The titi monkeys used taller and larger trees to sleep than the average trees at each study site and chose branches with high vegetation coverage and located in higher forest strata than those used during diurnal activity. Sleeping sites were randomly distributed within each group's home range, and the groups avoided using the same site on consecutive nights. The characteristics of the sleeping sites and the behavior of the titi monkeys suggest that predation avoidance, especially of scansorial carnivores, is an important factor driving sleeping site choice. We conclude that titi monkeys' strategy to avoid predation while sleeping depends on the presence of a heterogeneous forest stratum with large emergent trees and liana tangles, which offer a physical barrier against predators.

REGISTROS DE Callithrix aurita (Primates, Callitrichidae) E SEUS HÍBRIDOS NO PARQUE NACIONAL DO ITATIAIA

The occurrence of the Buffy-tufted-ear Marmoset Callithrix aurita in the Itatiaia National Park (INP) is considered rare. For over 50 years, there were no new records of the species within the PNI. In this study, after three years of surveys in the PNI (432h), no record of this species was obtained. Two other species were observed: Black-horned capuchin Sapajus nigritus (n=10) and Black-fronted Titi Monkey Callicebus nigrifrons (n=12). However, in 2015, when the surveys were already completed, I obtained two occasional records of C. aurita. The first as obtained in May in the surroundings of the PNI. In addition, a hybrid between C. aurita and C. penicillata (alien species) was photographed on a private property inside a forest area. Local residents confirmed the occurrence of the two species (native and hybrid) at the site and also reported rarity of native. The second record of C. aurita was carried out in October inside the PNI, at about 1100m a.s.l. In this occasion, I identified three individuals on an exotic pine tree. These new records of C. aurita, which is an endangered species in Brazil, reveal the importance of the PNI and surrounding areas for the species conservation and the need for specific studies mapping the native populations of C. aurita as well as of alien species. Knowledge about the ecology of alien Callithrix species is crucial to conservation actions for their control or eradication. Educational activities should also be carried out with residents of the surrounding PNI, with the objectives of preventing further releases of alien and participation of local people on control actions.

Foraging strategies of black-fronted titi monkeys (Callicebus nigrifrons) in relation to food availability in a seasonal tropical forest.

Many primates have to cope with a temporal scarcity in food availability that shapes their foraging strategies. Here we investigated the changes in diet, activity, and ranging behavior of a group of black-fronted titi monkeys (Callicebus nigrifrons) according to the availability of the main high-nutritional-density item in their diet and the foraging strategy adopted when this food is scarce. We monitored one habituated group using instantaneous scan sampling over 1year (533h of observation, 61days) in a seasonal tropical forest fragment (245ha). We simultaneously collected data on food availability with fruit traps. The titi monkeys consumed fleshy fruits, the main high-nutritional-density item of their diet, in accordance with its availability, and the availability of this item modulated the ingestion of vegetative plant parts, a relatively low-nutritional-density food. During high fleshy fruit availability, the titi monkeys consumed more fleshy fruits, flowers, and invertebrates. They also traveled more, but concentrated their activity in a central area of their home range. Conversely, during fleshy fruit scarcity, they increased the breadth of their diet, switching to one richer in seeds and vegetative plant parts, and with greater plant diversity. At the same time, they reduced most energy-demanding activities, traveling less and over shorter distances, but using their home range more broadly. Corroborating the optimal foraging theory, titi monkeys altered foraging strategies according to temporal food fluctuations and responded to low fleshy fruit availability by changing their diet, activity, and ranging behavior. The adoption of a low-cost/low-yield strategy allowed us to classify them as energy minimizers.

Local vs landscape drivers of primate occupancy in a Brazilian fragmented region

Understanding the drivers of species distributions in human-dominated landscapes is crucial for proposing sound conservation strategies. Primates are the most studied terrestrial vertebrate taxa, yet still, their response to forest loss and fragmentation widely varies among species. In this paper, we assessed the relative influence of local vs landscape features on occupancy of two primate species—the black-fronted titi monkey and the black-pencilled marmoset, in a Brazilian fragmented region. We created detection histories by performing repeated auditory surveys on 25 native vegetation patches. Then, we fitted occupancy models using habitat and GIS-based data as site covariates and weather conditions as detection covariates. We found that forest-like canopy elements are important for the titi monkey, a canopy-dependent species. Occupancy of marmoset, an opportunistic species, was also related to local elements, but in a lesser extent. In addition, we found that ignoring detectability in playback call surveys created a 20 % difference in occupancy estimates for the marmoset. We conclude that drivers of primate occupancy at the studied landscape rely mainly on local key habitat elements, so that on-ground conservation actions should not focus on habitat amount alone. Furthermore, we reiterate that primate researchers should explicitly account for imperfect detection to avoid substantial detectability bias.

Playback responses of socially monogamous black-fronted titi monkeys to simulated solitary and paired intruders.

Many birds and primates use loud vocalizations to mediate agonistic interactions with conspecifics, either as solos by males or females, or as coordinated duets. The extensive variation in duet complexity, the contribution of each sex, and the context in which duets are produced suggest that duets may serve several functions, including territory and mate defense. Titi monkeys (Callicebus spp.) are believed to defend their home range via solo loud calls or coordinated duets. Yet there are remarkably few experimental studies assessing the function of these calls. Observations of interactions between wild established groups and solitary individuals are rare and, therefore, controlled experiments are required to simulate such situations and evaluate the mate and joint territorial defense hypotheses. We conducted playback experiments with three free-ranging groups of habituated black-fronted titi monkeys (Callicebus nigrifrons) to test these hypotheses. We found that titi monkeys responded to the three conspecific playback treatments (duets, female solos, and male solos) and did not respond to the heterospecific control treatment. The monkeys did not show sex-specific responses to solos (N = 12 trials). Partners started to duet together in 79% of their responses to playback-simulated rivals (N = 14 calls in response to playback). Males started to approach the loudspeaker before females regardless of the type of stimulus. The strength of the response of mated pairs to all three conspecific treatments was similar. Overall, our results are consistent with the idea that black-fronted titi monkeys use their loud calls in intergroup communication as a mechanism of joint territorial defense.

Time-lags in primate occupancy: a study case using dynamic models

Species response to land-use changes are usually assessed by investigating factors affecting distribution, with a single snapshot in time. However, several processes can lead to a same pattern. Focusing on observed, short-term patterns limits our ability to make inferences about ecological processes and responses to environmental change over time. In this study, we assessed changes in occupancy of two primate species in southeastern Brazil, following a major habitat loss due to implementation of a hydroelectric dam. Occupancy was assessed before dam construction and 11 years after, while explicitly accounting for imperfect detection. We assessed the effect of forest patch size and isolation on occupancy and rates of extinction and colonization, driven by landscape modification. Then we calculated occupancy under metapopulation equilibrium and expected time-lags resulting from non-equilibrium. We compared two primate species inhabiting forest patches, the black penciled marmoset Callithrix penicilatta and the black-fronted titi monkey Callicebus nigrifrons, with markedly different ecological characteristics. Those differences may explain why occupancy dynamics were driven by distinct elements. A fast response to habitat changes was observed only for marmoset, an opportunistic species. However, non-equilibrium states and the possibility of time-lag effects were observed for titi monkey, a species dependent on forest habitat. Our analyses support the need to establish long term monitoring and assess system vital rates over time. A single snapshot in time may lead to erroneous interpretations of a species response to habitat alteration.

Do wild titi monkeys show empathy?

Abstract. We observed a putative case of empathy among wild black-fronted titi monkeys (Callicebus nigrifrons) from two different groups (D and R). In over 10 years of behavioural observations of five habituated groups of this species, only low levels of inter-group tolerance have been observed. However, on one day, we encountered the adult male from group D limping (poor hind limb motor coordination) as he travelled alone along the ground. Interestingly, we observed that members of group R did not express any agonistic behaviour towards this neighbouring male and apparently allowed this disabled individual to follow them in the forest for over 5 h. They stayed low in the forest (&lt; 2 m above the ground) and &lt; 10 m horizontally from the individual, and remained in visual contact with him. At the end of the day, this male from group D slept in the sleeping site of group R and was groomed by the adult female of group R. Such tolerance between members of different groups has never been previously observed in this species. Furthermore, group R exposed themselves to increased predation risk by staying close to the ground for protracted periods. The behaviour of group R could be interpreted by as a putative case of empathic responding in this species.

Vocal behavior of black‐fronted titi monkeys (Callicebus nigrifrons): Acoustic properties and behavioral contexts of loud calls

Loud calls can be heard over long distances due to their high amplitude and low frequency. These calls are commonly used for both within- and between-group communication in many bird and primate species. In the Neotropics, mated pairs of socially monogamous titi monkeys (genus Callicebus) emit conspicuous, coordinated loud calls. These vocalizations appear to play a role in territorial defense, a hypothesis derived from studies of only three of the 31 recognized Callicebus species. Here, we describe the acoustic properties and organization of the loud calls of black-fronted titi monkeys (Callicebus nigrifrons). We compare the behavioral and ecological contexts associated with these vocalizations to investigate their role in within- and between-group communication, resource defense, and mate defense. Black-fronted titi monkeys create loud calls by combining a finite number of syllables to form more complex phrases, which are assembled to compose long sequences of loud calls. Bioacoustic features distinguish the loud calls used in different contexts, involving communication within- and between-groups. We found support for the hypothesis that vocalizations used for between-group communication are cooperative displays used by the mated pair and other group members to regulate access to important food resources, such as fruits. On the other hand, we only found weak support for the mate defense hypothesis.

Titi monkey call sequences vary with predator location and type

Animal alarm calls can encode information about a predator's category, size, distance or threat level. In non-human primates, alarm calls typically refer to broad classes of disturbances, in some instances to specific predators. Here, we present the results of a field experiment with a New World primate, the black-fronted titi monkey (Callicebus nigrifrons), designed to explore the information conveyed by their alarm call system. Adults produced sequences consisting of two main alarm call types that conveyed, in different parts of the utterance, information about a predator's type and location. In particular, sequence compositions differed depending on whether the predator was a mammalian carnivore or a raptor, and whether it was detected in a tree or on the ground. This is the first demonstration of a sequence-based alarm call system in a non-human animal that has the capacity to encode both location and type of predatory threat.

Referential alarm calling behaviour in New World primates

Abstract There is relatively good evidence that non-human primates can communicate about objects and events in their environment in ways that allow recipients to draw inferences about the nature of the event experienced by the signaller. In some species, there is also evidence that the basic semantic units are not individual calls, but call sequences and the combinations generated by them. These two findings are relevant to theories pertaining to the origins of human language because of the resemblances of these phenomena with linguistic reference and syntactic organisation. Until recently, however, most research efforts on the primate origins of human language have involved Old World species with comparatively few systematic studies on New World monkeys, which has prevented insights into the deeper phylogenetic roots and evolutionary origins of language-relevant capacities. To address this, we review the older primate literature and very recent evidence for functionally referential communication and call combinations in New World primates. Within the existing literature there is ample evidence in both Callitrichids and Ce-bids for acoustically distinct call variants given to external disturbances that are accompanied by distinct behavioural responses. A general pattern is that one call type is typically produced in response to a wide range of general disturbances, often on the ground but also including inter-group encounters, while another call type is produced in response to a much narrower range of aerial threats. This pattern is already described for Old World monkeys and Prosimians, suggesting an early evolutionary origin. Second, recent work with black-fronted titi monkeys has produced evidence for different alarm call sequences consisting of acoustically distinct call types. These sequences appear to encode several aspects of the predation event simultaneously, notably predator type and location. Since meaningful call sequences have already been described in Old World primates, we suggest that basic combinatorial vocal communication has evolved in the primate lineage long before the advent of language. Moreover, it is possible that some of these communicative abilities have evolved even earlier, or independently, as there is comparable evidence in other taxonomic groups. We discuss these findings in an attempt to shed further light on the primate stock from which human language has arisen.