Late-Holocene asynchronous extinction of endemic mammals on the eastern Canary Islands

Abstract

The Lava mouse (Malpaisomys insularis), and the Canarian shrew (Crocidura canariensis) are endemic of the Eastern Canary Islands and islets. The former is extinct while Canarian shrew survives in the two main islands and two islets. In order to provide insights regarding causes and processes contributing to the extinction of these endemic mammals: (i) we established last occurrence dates for Lava mouse, and first records for two exotic species – House mouse (Mus musculus) and Black rat (Rattus rattus) – through direct ¹⁴C AMS dating of collagen from bones; (ii) we analysed recent material from Barn owl (Tyto alba gracilirostris) roosting sites to evaluate its impact on Canarian shrew in the presence of introduced rodents. The new data strongly suggest that the extinction of Lava mouse was the result of an accumulative process of independent disappearances (or ‘local extinctions’) affecting the isolated populations. The timing of the introduction of the Black rat on the main islands (before Middle Age European contact in Lanzarote and after Middle Age European contact in Fuerteventura) matches with the last occurrence dates for the presence of Lava mouse on these islands, and are very probably their cause. The losses of these Lava mouse populations occurred in an asynchronous way, spreading across at least six centuries. On small islands, hyperpredation emerges as the most plausible process to explain the disappearance of the Lava mouse in the absence of rat populations, although stochastic processes can not be definitively excluded.

Keywords

Canary Islands hyperpredation

Introduction

Island ecosystems have been traditionally used as a framework for the study of evolutionary phenomena (Whittaker and Fernández-Palacios, 2007). Archipelagos with islands that differ in geography, distance to mainland and faunal composition are ideal systems to tackle questions of adaptive radiation (Grant and Grant, 2007; James and Olson, 1991, 2003; Losos, 2009; Losos and Ricklefs, 2009; MacPhee and Flemming, 1999). Taking into account that many islands suffered great ecological changes after human arrival during the Holocene (i.e. habitat alteration, hunting, farming, and introduction of alien species including their parasites and diseases), accompanied by massive faunal extinctions (Boyer, 2008; Burney and Flannery, 2005; Olson and James, 1982; Steadman, 2006; Turvey, 2009a; van de Geer et al., 2010; Worthy and Holdaway, 2002), this framework could be used to provide insight into extinction causes and processes.

When the distribution of a species is restricted to a single island, the extinction process could be triggered by a single cause and take a very short time, perhaps only a few years in some cases (e.g. Wyatt et al., 2008). A limited population size and a reduced island area, both combined with a sudden expansion of the agent that caused extinction, are key conditions for such events. Species with small geographic ranges are more prone to extinction than those with larger distributions (Davidson et al., 2009). Archipelagos which have been inhabited by species now extinct emerge as ideal models to assess the tempo and mode of species extinction, as they permit inter-island comparisons. In addition, the understanding of species extinction on islands could help to prevent future biodiversity loss in islands ecosystems.

Among the Macaronesian archipelagos (Azores, Madeira, Selvagens, Canary Islands and Cape Verde at the North Atlantic Ocean), only the Canary Islands were inhabited by non-flying native mammals. As far as we know, they were inhabited by two genera and three species of endemic (and now extinct) rodents: two giant rats (Canariomys bravoi, C. tamarani) (Crusafont-Pairo and Petter, 1964; López-Martínez and López-Jurado, 1987) and the Lava mouse (Malpaisomys insularis) (Boye et al., 1992; Hutterer et al., 1988). Each of the two former species was distributed on a single island only (Tenerife and Gran Canaria, respectively), while the last species inhabited the two main islands of the eastern Canary Islands (Fuerteventura and Lanzarote; size 1660 and 846 km², respectively), and at least two smaller islets (Lobos and La Graciosa; 4.4 and 27.5 km², respectively) (Figure 1). A fourth species, the Canarian shrew (Crocidura canariensis), is the sole surviving non-flying mammal endemic to the Canary Islands, with living populations on Fuerteventura, Lobos, Lanzarote and Montaña Clara (1.3 km²). It suffered two local extinction events on the islets of La Graciosa and Alegranza (Figure 1) (Hutterer et al., 1987, 1992; Martín et al., 1984, 1990).

Figure 1.

Geographic situation of the Canary Islands showing the localities in Fuerteventura and Lanzarote where the recent diet of Barn owl (Tyto alba gracilirostris) was analysed (1: Jameos del Agua; 2: Montaña de La Arena; 3: Barranco de Los Molinos, 4: Barranco de Antigua), palaeontological (p) and archaeological (a) sites where the materials for dating where collected (I: Cueva del Llano; II: Cueva de Villaverde; III: Jameo de La Puerta Falsa; IV: El Bebedero; V: Tinache; VI: Montaña Amarilla and VII: Old roost), and the distribution of micromammals on the eastern islands and islets. MI: Lava mouse (Malpaisomys insularis); CC: Canarian shrew (Crocidura canariensis); MM: House mouse (Mus musculus); RR: Black rat (Rattus rattus). †: extinct; *: exotic.

Radiocarbon dates indicate that the first settlers reached the Canary Islands from North Africa some time between 756 cal. bc and 313 cal. ad (Alcover et al., 2009). According to the available archaeological evidence, the aboriginals introduced goat (Capra hircus), sheep (Ovis aries), pig (Sus scrofa), dog (Canis familiaris) (Atoche, 2009; Cabrera et al., 1999) and House mouse (Mus musculus) (Alcover et al., 2009). Europeans arrived in the archipelago at the beginning of the 14th century ad (Aznar et al., 2006).

Lava mouse extinction was previously studied on Fuerteventura, where the species survived at least until the 13th century ad. This date links its extinction directly to the introduction of the Black rats via European settlement (Rando et al., 2008). Previously, Lava mouse had survived the arrival of aboriginals with their livestock and resulting habitat alterations on Fuerteventura, and also the introduction of the House mouse, which took place some time between 756 cal. bc–313 cal. ad (Alcover et al., 2009).

Black rat bones have been reported from archaeological sites of Lanzarote (from levels containing material attributed to Roman culture; Atoche, 2009; Criado and Atoche, 2003). In contrast, they have never been obtained from the pre-European sites of the remaining Canary Islands. Additionally, Black rats are not present on the small islets where the Lava mouse was present. Consequently, the cause of Lava mouse disappearance on these islets should have been different from the one affecting the main islands. By contrast, the House mouse currently inhabits all islands and islets where Lava mice were formerly present (Fuerteventura, Lobos, Lanzarote, and La Graciosa), as well as the islet of Alegranza (where no evidence of an earlier presence of the Lava mouse exists). The only islet where the House mouse is not present is Montaña Clara (Figure 1).

This puzzling situation, which includes (i) an extinct endemic species on different islands and islets (Lava mouse), (ii) an extant endemic species (Canarian shrew) surviving on both the main eastern Canary Islands and on one islet, while having disappeared from two other islets, (iii) the occurrence of different combinations of alien mammals on islands and islets, and (iv) an extant endemic subspecies of Barn Owl (Tyto alba gracilirostris), a predator of small mammals (Del Hoyo et al., 1999; Martín and Lorenzo, 2001), provides a system suitable for exploring the causes of native mammals disappearance on geographically close islands of different size.

This work aims to provide insights into the causes and processes contributing to the population decline of Canarian endemic mammals. For this purpose, we obtained (i) last occurrence dates for an extinct endemic species, the Lava mouse, (ii) first occurrence dates for alien rodents, House mouse and Black rat, on different islands and islets through direct ¹⁴C AMS dating of bone collagen, and (iii) recent material from roosting sites of the Barn owl in order to investigate the latter’s impact on the endemic shrew (Crocidura canariensis) in the presence of introduced rodents. These data are used to explore chronologies and causes of local disappearances, key topics for understanding current insular biodiversity loss.

Methods

Samples for dating were selected according to the following criteria: (i) unequivocal taxonomic identity, (ii) good overall quality of bone preservation, and (iii) stratigraphic position in the deposit, sampling the deepest recorded bones for alien species and the uppermost ones for the extinct taxa. Selected samples were dated by accelerator mass spectrometry (AMS) of ¹⁴C derived from bone collagen. We avoided dating of samples containing different species. Bones were cleaned and pre-treated by the Longin method (Gillespie et al., 1984). In addition, we incorporated previously published dates obtained with the same methodology (samples: KIA-30983/ 30994/ 36469/ 36470; Alcover et al., 2009; Rando et al., 2008). A description of each sample is given in Table 1.

Table 1.

Radiocarbon dates of bones of Lava mouse (Malpaisomys insularis), House mouse (Mus musculus) and Black Rrat (Rattus rattus) from sites in the Eastern Canary Islands. Conventional radiocarbon age (BP) and 2σ calibration interval (cal. bc or ad) are given. 2σ calibration intervals were calculated using OxCal 4.0 program and IntCal04.14C calibration curve.

	Island/islet	Lab code	Site	Radiocarbon age (BP)	2σ Calibration interval (cal. bc/ad)	C/N	δ¹³C (‰)	Dated material
Lava mouse	F	KIA-30983	Cueva del Llano	670±35	ad 1271–1394^L	2.8	−18.33	Assemblage of a complete left jaw without M₁, 2 humeri without proximal epiphysis, 1 fragmented pelvis, 2 femora without distal epiphysis, 1 tibia without proximal epiphysis
Lava mouse	L	KIA-36469	Jameo Puerta Falsa	2075±25	174–4 bc^L	3.2	−15.98	Assemblage of a complete left jaw without incisor, 2 left and 1 right maxillae, 1 radius, 2 fragmented femora
Lava mouse	G	KIA 40848	Montaña Amarilla	5775 ± 35	4714–4541 bc^L	3.3	−17.31	Assemblage of three fragmented left jaws, one fragmented right jaw and 4 fragmented left maxillae
House mouse	F	KIA-30994	Cueva de Villaverde	1415±40	ad 565–669^F	2.8	−18.05	A skull lacking of its occipital part and 1 femur
House mouse	L	KIA-36470	El Bebedero	1815±25	ad 128–313^F	3.2	−19.11	Assemblage of 8 I₁, 2 I¹, 9 humeri, 9 femora and 11 tibiae
House mouse	G	*WK-28572	Old roost	1275±31	ad 661–810^F	3.2	−15.8	Assemblage of 19 left and 15 right jaws, 2 left maxillae, 1 humerus, 3 femora and 1 tibia
Black rat	L	KIA-36265	Tinache	1460±25	ad 580–650^F	3.2	−17.93	Assemblage of 1 left and 1 right fragmented jaws, 1 left and 1 right fragments of maxillae
Black rat	L	KIA 40843	Tinache	1125 ± 20 BP	ad 885–980	3.2	−18.94	1 right jaw and 1 femur

C/N: Carbon-to-Nitrogen ratio. ^Ffirst known record and ^Llast known occurrence at each island or islet. Radiocarbon ages were measured at the ¹⁴C Laboratory of the Royal Institute for Cultural Heritage (Brussels, Belgium) and *Radiocarbon Dating Laboratory of the University of Waikato (Hamilton, New Zealand). F: Fuerteventura; L: Lanzarote; G: La Graciosa. Samples KIA-30983/ 30994/ 36469/ 36470 from Alcover et al. (2009) and Rando et al. (2008).

The ¹⁴C ages are expressed as 2σ intervals (i.e. the ranges of the 95.45% confidence intervals); interpretations are based on total analytical range, i.e. the entire interval between extreme values (see Alcover et al., 2001; Bover and Alcover, 2003; Ramis et al., 2002; Zilhão, 2001). Calibrated years are presented as cal. bc/cal. ad. Ages were calibrated using version 4.1.3 of the OxCal programme (Bronk-Ramsey, 2009) and IntCal04 ¹⁴C calibration curve.

In order to assess the impact of Barn owls on native shrews in the presence of introduced rodents, we analysed complete and decayed pellets at three roosting sites in Fuerteventura (Montaña de La Arena, Barranco de los Molinos and Barranco de Antigua) and one in Lanzarote (Jameos del Agua) (Figure 1). Owing to the fact that the analyses were performed on both complete and decayed pellets, it is impossible to know the number of analysed pellets.

To obtain quantitative information about the importance of each prey species in the diet in terms of biomass, we used specimens from the vertebrate collection of the Zoology Department of La Laguna University (DZUL) to estimate the biomass of the Canarian shrew, the House mouse and the Gecko (Canarian shrew (Crocidura canariensis) 8±0.7 g (n = 4); House mouse (Mus musculus) 14±4 g (n = 48); Gecko (Tarentola angustimentalis) 7±3.1 g (n=15)), data from Cramp and Perrins (1994) for passerine birds (Bucanetes githagineus) 18±1.9 g (n=13), and our data to estimate the biomass of Black rat (Rattus rattus) 85±55 g (n = 29).

Sampling stations

In order to obtain information on last (endemic) and earliest (alien) occurrence records for the species under consideration, we prospected places suitable for ancient owl pellet accumulation on Lobos, La Graciosa and Lanzarote (Figure 1) lava fields (locally known as ‘malpaíses’, in the singular, ‘malpaís’), fissures, lava tubes, and caves. In addition, we visited two archaeological sites on Lanzarote where the presence of Black rat bones has been reported (Atoche, 2009; Criado and Atoche, 2003) in order to verify this record through direct ¹⁴C AMS dating. The field work was performed during 2008 and 2009 in two campaigns of about one week. Previous data obtained in Fuerteventura have been incorporated for comparative purposes.

Samples used in this paper come from four palaeontological (Cueva del Llano, Jameo de la Puerta Falsa, unnamed cave at Montaña Amarilla and one old roost close to Montaña Amarilla) and three archaeological sites (Cueva de Villaverde, El Bebedero and Tinache) (see Figure 1 for their geographic location).

Cueva del Llano (Fuerteventura)

A Pleistocene volcanic tube (Fúster and Carracedo, 1979) situated in the north of the island of Fuerteventura (Figure 1), with a sedimentary infilling. Close to the entrance, in its southern part, there is a huge microvertebrate bone accumulation. Bones of Lava mouse, Canarian shrew, extinct Canarian quail (Coturnix gomerae), other birds, Fuerteventura gecko (Tarentola angustimentalis), and Atlantic lizard, (Gallotia atlantica) are present. The very rich upper levels of the site were formed by direct accumulation of owl pellets, apparently without further transport (Alcover et al., 2009; Castillo et al., 2001). The sample from this site came from the upper level 9.1, and was collected in the section of this level (see Alcover et al., 2009, for details of the stratigraphy).

Jameo de la Puerta Falsa (Lanzarote)

Infilled fissure containing sediment and a few bones. Remains of Lava mouse and Canarian shrew are present. The fissure is located inside the Jameo (‘jameo’ meaning a roof collapse of a lava tube), which is situated in the lava field produced by the Upper Pleistocene eruptive activity of Volcán de La Corona (north of Lanzarote, Carracedo et al., 2003; Coello et al., 1992) (Figure 1). No differentiated stratigraphic units can be identified.

Cave at Montaña Amarilla (La Graciosa)

This unnamed small (≈ 2 m long) cave is located in the southern side of the top of Montaña Amarilla (La Graciosa Islet) (Figure 1). Bones of Lava mouse, House mouse and Canarian shrew were collected directly from the floor surface where no sediments were accumulated.

Old roost (La Graciosa)

It is an infilled fissure containing sediment and bones of House mouse, Lava mouse and Canarian shrew. This site is located on La Graciosa Islet, at the foot of Montaña Amarilla, in the west side of this mountain (Figure 1). No differentiated stratigraphic units can be identified. Both Montaña Amarilla and this site are of Upper Pleistocene age (Coello et al., 1992; de la Nuez et al., 1997).

Cueva de Villaverde (Fuerteventura)

This Pleistocene volcanic tube is located in the north of Fuerteventura (Coello et al., 1992; Meco, 1992) (Figure 1). The archaeological remains of this site are located inside and outside the cave. Inside the cave four levels had been identified, the archaeological remains are present in the uppermost (Meco, 1992). Bones of House mouse, Lava mouse, Canarian shrew, Fuerteventura gecko, several species of birds and livestock are present (Carrascosa and López-Martínez, 1988; Hutterer et al., 1987, 1988). The bones of House mouse for this paper were collected at the bottom of the archaeological level. The sample was collected in the exposed section of this level (Alcover et al., 2009).

El Bebedero (Lanzarote)

This outdoor archaeological site is situated in a field depression or ‘Caldera’ of Pleistocene age (Coello et al., 1992), located in the center of the island of Lanzarote (Criado and Atoche, 2003) (Figure 1). Five levels containing archaeological remains had been identified (Atoche et al., 1995; Criado and Atoche, 2003). Bones of House mouse, Lava mouse, Canarian shrew, Black rat (Rattus rattus), Fuerteventura gecko, several species of birds and livestock are present (Criado and Atoche, 2003). Studied samples of House mouse for this paper are from the lowermost level V. The sample was collected in the exposed section of this level (Alcover et al., 2009).

Tinache (Lanzarote)

Close and similar in morphology and age to El Bebedero, five archaeological levels have been identified. Remains of the same animal species than in El Bebedero had been obtained (Atoche, 2009). The two samples of rat bones for this paper are from level IV, and they were collected in the exposed section of this level from an archaeological pit.

Results

Bones of Lava mouse, Canarian shrew, and House mouse from ancient owl-pellet accumulations in Lanzarote and La Graciosa were obtained. In contrast, at Tinache (Lanzarote) bones of the Black rat were found in sections of archaeological pits (Figure 2a) at levels in which bones of livestock and aboriginal pottery were also present. On Lobos only recent owl-pellet accumulations were found containing mainly of House mouse and Canarian shrew, although bones of Lava mouse were sporadically recovered from several places (fissures and surface findings) on the islet.

Figure 2.

(a) Right mandible and fragment of right femur of Black rat (Rattus rattus) from the archaeological site of Tinache (Lanzarote); (b) Fragments of four mandibles (three lefts and one right) and four maxilla bones (left side) of Lava mouse (Malpaisomys insularis) from an ancient Barn owl (Tyto alba gracilirostris) pellet accumulation at Montaña Amarilla (La Graciosa). Both samples were dated through ¹⁴C AMS (lab codes: KIA-36265 and KIA 40848, respectively). Scale bars = 2 cm.

The radiocarbon ages obtained are given in Table 1. Despite the very recent aspect of the bones of Lava mouse from Lanzarote and La Graciosa (Figure 2b), this material exceeded two millennia (radiocarbon ages, 174–4 cal. bc and 4714–4541 cal. bc, respectively). These two samples represent today the last known records of the Lava mouse on these islands. In our approach, the disappearance of these populations can be said to have taken place later than 174 cal. bc and 4714 cal. bc, respectively.

The House mouse material from Lanzarote, La Graciosa and Fuerteventura is younger than 2000 years ago (earliest occurrence dates for each island, 128–313 cal. ad, 661–810 cal. ad, and 565–669 cal. ad, respectively). The two samples of Black rat bones from Lanzarote clearly pre-date European contact (580–650 cal. ad and 885–980 cal. ad). This early presence is in contrast to its late documentation from the remaining Canary Islands, where Black rat bones have never been obtained from aboriginal levels. These dates indicate that the introduction of this exotic rodent into Lanzarote took place before 650 cal. ad.

The House mouse is the most important prey in the present diet of barn owls on Fuerteventura and Lanzarote (58–81% of biomass), while the Canarian shrew is less important (2.3–4.6%). The remaining prey species (black rat, reptiles and birds) are of intermediate importance (Table 2).

Table 2.

Percentage of current preys (P) and biomass consumed (B) by Bar owl (Tyto alba gracilirostris) in three localities of Fuerteventura (Barranco de Antigua, Barranco de Los Molinos and Montaña de la Arena) and one in Lanzarote (Jameos del Agua).

Localities	Total preys	Canarian shrew		House mouse		Black rat		Reptiles		Birds
		% P	% B	% P	% B	% P	% B	% P	% B	% P	% B
Bco. Antigua	295	3.7	2.3	53.6	58	2	13.3	35.6	19.3	5	7.1
Bco. Molinos	214	4.2	2.6	74.8	81	0.5	3.1	17.7	9.5	2.8	3.8
Mta. Arena	365	5.2	3	77.8	79	1.4	8.4	13.4	6.8	2.2	2.8
Jameos	5080	8.4	4.6	68.6	66	3.4	19.9	19.1	9.2	0.5	0.6

Discussion

The new radiocarbon ages presented here (Table 1) strongly suggest that the extinction of the Lava mouse was the result of an asynchronous process of local disappearances, triggered by different causes on the large islands as compared to the small islets.

The disappearance of the Lava mouse on the large islands: Fuerteventura and Lanzarote

The Lava mouse survived on Fuerteventura at least until the 13th century (1271–1394 cal. ad). The overlap of this confidence interval with European presence in the Canary Islands (14th century; Aznar et al., 2006) suggests a relationship between both events. The introduction of Black rats together with their parasites, diseases and even perhaps vectors by European settlers emerges as the most reasonable hypothesis explaining endemic extinctions (Rando et al., 2008). This conclusion is strengthened by the fact that on Fuerteventura the Lava mouse coexisted with the introduced House mouse (Carrascosa and López-Martínez, 1988) for more than six centuries according to dates directly obtained from bones of both species (from 669 cal. ad to 1271 cal. ad; Alcover et al., 2009).

A similar pattern emerges on Lanzarote, where the Black rat was also introduced. Nevertheless, on this island the Black rat presence is documented before 650 cal. ad on the basis of radiometrically dated bone. Thus, the available ¹⁴C evidence points to a different chronology for the disappearance of the Lava mouse on each of the large islands. In contrast to Fuerteventura, the most recent bones of the Lava mouse on Lanzarote date from the 2nd century ad (174 cal. BP) (Table 3). The rather early ages for both the last record of the Lava mouse and the first occurrence of the rat point to a similar relationship between both events (extinction and introduction) as in Fuerteventura, but in an asynchronous way and with a temporal difference of at least six centuries (Figure 3) – i.e. difference between 650 cal. ad for first occurrence of Black rat on Lanzarote and last record of Lava mouse on Fuerteventura (1271 cal. ad). Asynchronous extinction in mammals is not an unknown phenomenon, although it has been reported only a few times, i.e. for the Woolly mammoth (Mammuthus primigenius) (Vartayan et al., 1993) and for genera of Xenarthra (Steadman et al., 2005). In both cases, extinction followed the first presence of humans.

Table 3.

Areas (km²), last known records of Lava mouse (Malpaisomys insularis), first known records of House mouse (Mus musculus) and Black rat (Rattus rattus) and locals extinctions of Canarian shrew (Crocidura canariensis) in eastern Canary Islands and Islets.

Island/Islet	Area km²	Lava mouse last records	Canarian shrew	House mouse first record	Black rat first record
Fuerteventura	1660	1271–1394 cal. ad	✓	✓ 565–669 cal. ad	✓ 14th–15th century
Lobos	4.4	†	✓	✓?	−
Lanzarote	846	174–4 cal. bc	✓	✓ 128–313 cal. ad	✓ 580–650 cal. ad
La Graciosa	27.5	4714–4541 cal. bc	†	✓ 661–810 cal. ad	−
Montaña Clara	1.3		✓	−	−
Alegranza	10.2		†	✓?	−

✓: Living population; †: extinct population at unknown time; –: the species never had been established in that island or islet; ?: unknown first record.

Figure 3.

Schematic summary of ¹⁴C AMS confidence intervals for the last records of Lava mouse (Malpaisomys insularis; MI), the first occurrences of the House mouse (Mus musculus; MM) on Lanzarote and Fuerteventura and the first occurrence of Black rat (Rattus rattus; RR) on Lanzarote Island. *European presence on the Canary Islands; the introduction of Black rat into Fuerteventura took place after this date.

For Lanzarote we lack radiocarbon evidence for the coexistence of Lava mouse and House mouse; the earliest record for the latter is 313 cal. ad (Table 1 and Figure 3). However, there is stratigraphic evidence for their coexistence on the island (as they did on Fuerteventura; Alcover et al., 2009) some time before the arrival of rats, as indicated by their occurrence in the earliest level at El Bebedero archaeological site, where bones of both species are present in a clear archaeological context (Criado and Atoche, 2003). The lack of evidence for coexistence of Lava mouse and Black rat on both islands should not be interpreted as a proof of absence of contact. It is possible that the introduction of Black rats, along with their parasites and diseases, led to a very quick disappearance of the Lava mouse, perhaps in too short a time to leave any archaeological or palaeontological trace. Remarkably, sudden extinction of insular rodents has been reported for the two endemic rodents of Christmas Island (Rattus macleari and R. nativitatis), which disappeared within nine years after the introduction of murid trypanosomes by Black rats (Wyatt et al., 2008). Sudden extinctions seems to be common among native island birds (see Flannery and Schouten, 2001; Fuller, 2000). Well-dated archaeological sites across Oceania indicate the frequent association of human arrival and the almost instantaneous disappearance of endemic species sometimes over a time interval less than the statistical error associated with radiometric dating and therefore too rapid to be resolved by this technique (see Steadman, 2006; Turvey, 2009b).

Small populations are the most widely reported target of disease-induced extinction in natural populations (De Castro and Bolker, 2005). This way, the introduction of diseases and vectors, could have played a role in the extinction of Hawaiian birds. One species of Plasmodium is present from sea level to treeline, concentrated in mid-elevation ranges where vectors and native birds had the greatest overlap, having restricted the distribution of some native birds because of their higher susceptibility to malaria (Atkinson et al., 1995, 2000; van Riper III et al., 1986).

The stratigraphy of the El Bebedero archaeological site supports the sudden disappearance of the Lava mouse on Lanzarote: Lava Mouse bones are present in level 5 (the lowest level of the section), while they are absent from the contiguous and younger levels 4 and 3, where bones of rats are present (Criado and Atoche, 2003). The absence of domestic cat (Felis catus) from the archaeological record of Lanzarote and Fuerteventura should also be noted.

The early disappearance of the Lava mouse on Lanzarote coincides with the lack of remains of the Lava shearwater (Puffinus olsoni) from the archaeological sites on this island. This bird survived on Fuerteventura until at least the 13th century, as did the Lava mouse. Both disappearances were associated with the introduction of the Black rat into Fuerteventura (Rando and Alcover, 2008; Rando et al., 2008). The presence of livestock, and the absence of rats from the oldest level of the archaeological site of El Bebedero (Criado and Atoche, 2003) strongly suggest that rats were not among the first alien species introduced into the island. Rats were therefore probably introduced some time after the first human settlers arrived. The ¹⁴C ages indicate that the House mouse arrived on the eastern Canary Islands sometime between 756 cal. bc and 313 cal. ad, likely as stowaways on the boats of the first settlers (Alcover et al., 2009). Later, rats were probably introduced by the Romans. Some metal, glass, and pottery fragments of Roman origin have been excavated on Lanzarote (Atoche et al., 1995), and materials attributed to Roman culture were found on La Graciosa and the now submerged shoreline of Lanzarote, as well as on Gran Canaria and Tenerife, although the attribution of some of these objects to the Roman culture has been questioned by several authors (see Cabrera et al., 1999; Chávez and Tejera, 2010; and references therein). Taking into account that Black rats were dispersed throughout the western Mediterranean by the Romans (McCormick, 2003) between the 4th and 2nd century bc (Vigne and Valladas, 1996), the latter could have been also responsible for an early introduction of rats into Lanzarote. The total absence of both Roman objects and Black rat remains in the archaeological record of the other Canary Islands seems to indicate sporadic visits rather than frequent contacts.

The recent introduction into the Canary Islands of the Brown rat (Rattus norvegicus) (18th century; Nogales et al., 2006) should be considered. Brown rat was absent during the extinction process of native mammals, precluding its role in the process. The Brown rat is currently distributed over the main islands but is absent from the islets.

The disappearance of the Lava mouse on the islets: Lobos and La Graciosa

The absence of Black and Brown rats on these islets indicates that the collapse of the Lava mouse populations is unrelated to these species.

Ecological differences among smaller and larger eastern Canary Islands have been reported (e.g. Illera et al., 2006). Additionally, a great difference among these islands and islets is area (Fuerteventura, 1660 km² and Lanzarote, 846 km², versus Lobos, 4.4 km² and La Graciosa, 27.5 km²; Figure 1 and Table 3). All these different conditions – area and ecological traits – suggest that the population size of the Lava mouse on these islands and islets should have been likewise markedly different.

Two possible extinction causes emerge from this scenario: (i) a stochastic event due to the fact that small populations are more vulnerable to climatic or geological disaster than the larger ones; (ii) a hyperpredation process by local barn owls affecting the Lava mouse could have taken place after the introduction of House mouse into the islets.

Although the only date for Lava mouse bones from La Graciosa is 4714–4541 cal. bc, it cannot be ruled out that this population (and that of Lobos) survived at least until the first major ecological impact of the Holocene, i.e. the introduction of the House mouse. The chronology of House mouse introduction into Lobos is unknown, but in La Graciosa the introduction took place in aboriginal times, before ad 661 (Table 1). Curiously, there were no aboriginal settlers on the islets at the moment of European arrival (14th century) (Torriani, 1978).

Once settled, the House mouse population is likely to have reached very high densities, particularly in the absence of rats limiting their dispersion (Angel et al., 2009). On the other hand, the Lava mouse, like other insular rodents (Adler and Levins, 1994), may have had a slower reproduction rate than the House mouse. In one plausible scenario, small islets of limited carrying capacity with (i) small populations of the Lava mouse and (ii) high densities of the House mouse (an invasive species well adapted to high predation pressure and with a high reproductive potential), a hyperpredation process affecting the Lava mouse could have taken place.

Such a process predicts that an introduced prey species, well adapted to high predation pressure because of its high reproductive potential, can induce the disappearance of another, local, prey species through an increase in the population size of the predator (Courchamp et al., 2000; Moleón et al., 2008; Smith and Quin, 1996; Taylor, 1979). Hyperpredation has strongest effect on species with low intrinsic growth rate living in an environment with low carrying capacity (Courchamp et al., 2000), and it explains the extinction of some species of birds and mammals (Smith and Quin, 1996; Taylor, 1979). This process was originally described for systems where both the new prey and the predator were introduced species (Courchamp et al., 2000; Smith and Quin, 1996; Taylor 1979).

Before the introduction of the House mouse into the eastern Canary Islands the Lava mouse was the most important prey for the Barn owl, comprising 78.5–90.3% of the biomass of its diet (Castillo et al., 2001). Today, the most important prey items of the Barn owl are alien rodents, with the House mouse being the principal source of biomass consumed (between 58% and 79%; Table 2). Owing to the continued presence of Barn owls on the islets, and because their density depends on prey density (Del Hoyo et al., 1999; Snow and Perrins, 1998), Barn owls could have reached high densities after the introduction of the House mouse. Additionally, an introduced predator, the domestic cat, could also have played a role in the disappearance of endemic mammals. Nevertheless, cats show a strong preference for rabbits on these islands, while their impact on micromammals is low (91.5% rabbit versus 8% rodent biomass in the diet; Nogales and Medina, 2009).

Subsequent to the introduction of the House mouse, a hyperpredation process affecting autochthonous small mammals by Barn owl is to be expected. This could explain the local disappearance of the Lava mouse on the islets in the absence of alien predators. Likewise, the local disappearance of the Canarian shrew on La Graciosa and Alegranza could have had the same cause. Two facts support our interpretation: (i) shrews are abundant in the single islet (Montaña Clara) where House mouse and cat have never been present (Martín et al., 1990), and (ii) the slow reproduction rate of the Canarian shrew, with a mean litter size of 2.1 and 1.5 for the populations on Fuerteventura and Montaña Clara, respectively (Hutterer et al., 1992). An exception to this pattern is the islet of Lobos where both House mouse and Canarian shrew are present (Hutterer et al., 1987; Martín et al., 1990), although the shrew’s abundance is very low (R. Hutterer, personal observations). An undated bone assemblage collected in 1990 from a fissure filling on Lobos (R Hutterer and J Michaux, unpublished data, 1990) seems to indicate that shrews were once much more abundant on the islet. It should, however, be noted that before House mouse introduction, the Canarian shrew was already a minor component of the Barn owl diet, just as it is today (< 7% and ≤ 3% of the biomass, respectively, Table 2). A low preference may indicate that owls had a lower impact on shrews than they had on the Lava mouse populations.

Conclusions

The palaeontological and archaeological record, and the radiocarbon dates seem to indicate that the Black rat arrived on Lanzarote and Fuerteventura with a time difference of at least six centuries. Regardless, although ¹⁴C AMS data do not definitively demonstrate asynchronic extinction, the evidence presented herein strongly suggests that, on these two islands, the disappearance of the Lava mouse was triggered by the same cause, the introduction of Black rats, but asynchronously (Figure 3). The last record of the Lava shearwater in Fuerteventura (1270 cal. ad) and the lack of remains of this species from the archaeological record of Lanzarote seem to indicate a similar asynchronous disappearance.

The absence of rat populations from the islets of Alegranza and La Graciosa on which the Lava mouse occurred indicates that its disappearance was triggered by other causes. Stochastic events (demographic and environmental) and hyperpredation processes are putative causes to explain the local disappearance of Lava mouse at the islets. These considerations suggest that a possible introduction of the House mouse into Montaña Clara islet could threaten the survival of the local population of the Canarian shrew, the only endemic population surviving in the absence of any alien mammal.

Footnotes

Acknowledgements

We thank the Area de Patrimonio of the Cabildo de Lanzarote and Fuerteventura, especially Nona Perera and Nacho Hernández. Thanks also to Miquel Trias, Aurelio Martín, and F. García-Talavera for their help, and to Mark van Strydonck and Mathieu Boudin of the Royal Institute for Cultural Heritage (Brussels). Gustav Peters kindly provided linguistic advice. Publication No. 2011-120, ISE-M CNRS 5554.

This work was supported by Spanish DGICYT Research Projects CGL2007-62047/BTE (Cronología y causas de las extinciones de vertebrados autóctonos en Canarias y Baleares: un análisis comparativo. II) and CGL2010-17889 (Mecanismos, procesos y patrones en los cambios pleistocénicos y holocénicos en la biodiversidad insular: Macaronesia versus Baleares).

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