Review Article |
Corresponding author: Claudio Ghittino ( c.ghittino@izsum.it ) Academic editor: Lyubomir Penev
© 2015 Claudio Ghittino, Enrico Busato, Achille Casale.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ghittino C, Busato E, Casale A (2015) Re-establishment of Carabus (Cathoplius) aliai Escalera, 1944 as a separate valid species (Coleoptera, Carabidae). ZooKeys 496: 61-84. https://doi.org/10.3897/zookeys.496.9428
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Carabus (Cathoplius) aliai was described as a separate species by Escalera in
Carabus ground beetles, Saharan desert endemism, Atlantic element, life cycle, hybridization
The subgenus Cathoplius C.G. Thomson, 1875 within the Genus Carabus Linnaeus, 1758 forms a very homogenous and peculiar lineage of strictly snail-predating ground beetles adapted to live in arid habitats with scarce xerophilous vegetation along the Moroccan Atlantic coast (
Carabus (Cathoplius) aliai is a desert-dwelling taxon that was first described by Manuel Martinez de la Escalera in August 1944. This description was based on the examination of only one specimen, a female found by the Spanish geologist Manuel Alía in April 1943 in El Khaloua which is 15 km north of present Abteh, in former Cape Juby strip, southern territories of the Spanish protectorate in Morocco (
Dr Joaquin Mateu, to whom this contribution is dedicated, really discovered and first studied C. aliai. In November 1944, he collected a further seven specimens (five males and two females) south of Laâyoune, in an area comprised between Izik plateau, Lemsid (Ougnit) and Metmarfag (Asreifa) to the west and Bou Kra to the east. This area is characterized by the presence of “graras”, land depressions where water cumulates during the raining season, allowing a certain vegetation to grow and consequently snails to dwell in. It was here that C. aliai specimens were observed during early morning or late afternoon while running, mating or eating snails of the family Helicidae. In addition to the biogeographic and biological notes, in his paper on the carabid beetles of Spanish Sahara,
Some years later, French entomologists dealing with the Moroccan carabid fauna reconsidered C. aliai as a subspecies of C. (Cathoplius) stenocephalus Lucas, 1866 (
Modern catalogues and checklists of the Genus Carabus either consider C. aliai as a “strong” subspecies of C. (Cathoplius) stenocephalus (
Field observations on Carabus (Cathoplius) aliai Escalera, 1944 are the results of nine surveys (March–April 1992; December 1999; January 2000; January, February–March & April 2006; November 2008; January & December 2010) carried out in the Guelmim, Tan-Tan and Laâyoune areas, southern Morocco. From December 14–19, 2010, one of the authors (C. G.) sampled 11 adult specimens (7 males and 4 females) and 10 larvae (1 first instar and 9 second instars) of this taxon on the Tan-Tan northern plateau (Hameidia Tellia: 2 km west of Tan-Tan city, 90–110 m a.s.l., 28°27'13"N; 11°07'53"W, and 7 km west of Tan-Tan city, 190 m a.s.l., 28°26'21"N; 11°10'30"W, in Ben Khlil rural commune, Tan-Tan province). In addition, observations on the behavior of specimens in their natural environment were recorded.
Life cycle investigations included the maintenance and breeding of C. aliai adults and larvae in the laboratories of the State Veterinary Institute (IZSUM) in Terni, Italy. Breeding activities started on 21 December 2010 and ended on 30 April 2013. The breeding methodology used was basically that reported by
Carabus aliai mating pairs were maintained in a 50 × 30 × 30 cm (length × width × height) transparent terrarium with a perforated top for aeration. A 15 cm substrate, composed of a mixture of argillaceous soil (40%) and sand (60%) was placed on the bottom of each terrarium. One third of the substrate surface was covered with a layer of moss. The substrate was kept moist by periodic spraying with water. Adults were ad libitum fed with live Theba pisana pisana (O.F. Müller, 1774) snails. In order to compare their life cycles, C. (Cathoplius) stenocephalus ifniensis adults (previously collected on the beach of Sidi Ifni city, 10 m a.s.l., 29°23'52"N; 10°10'40"W, Sidi Ifni province, central Morocco) were bred in parallel with C. aliai. Two mating pairs of both taxa were introduced in the terrariums on 21 December 2010 and two others on 1 December 2011 as a control group.
Larvae were reared individually in cylindrical opaque plastic containers (10 cm in diameter, 13 cm height) filled with 9 cm of the same substrate and kept at the same temperature as adults. Larvae were fed with live T. pisana pisana snails of the appropriate size (shell width 10–20 mm). In each container, a piece of bark [5 × 3 × 1(h) cm] was placed on top of the substrate as a shelter for the larva. Neo-adults were kept in mini-terrariums [20 × 12 × 15(h) cm] with a 5 cm substrate and a layer of moss, and ad libitum fed with live T. pisana pisana snails until their complete sclerification.
Following pure breeding, hybridization experiments between virgin C. aliai and C. stenocephalus ifniensis were carried out. Four mating pairs of the combination C. aliai ♂ × C. stenocephalus ifniensis ♀ (AIF1) and four of the combination C. stenocephalus ifniensis ♂ × C. aliai ♀ (AIF2) were bred at the same temperatures and at the same photoperiod previously reported, starting from December 1, 2011. Due to the different size between C. aliai (generally smaller) and C. stenocephalus ifniensis (generally larger), small females of C. stenocephalus ifniensis and large males of C. aliai were used to obtain AIF1 hybrid, while large females of C. aliai and small males of C. stenocephalus ifniensis were used to obtain AIF2 hybrid. Once obtained, AIF1 and AIF2 hybrids were then crossed with one another to investigate their fecundity. The F1 crossbreeding experiments were done in quadruplicate starting on December 3, 2012.
Representative specimens of C. aliai and C. stenocephalus ifniensis used for comparative morphological studies are conserved dry or under alcohol in authors’ collections.
Morphology of adults. Morphological differences observed among adults of the various Cathoplius taxa were in agreement with those reported by
The head was slender in C. aliai and broad in C. stenocephalus ifniensis. The pronotum was narrow and elongated, longer than wide, with a very reduced lateral furrow in C. aliai, while it was transverse, wider than long, with a developed lateral furrow in C. stenocephalus ifniensis. On average, the ratio between length of pronotum and maximum width of pronotum (PL/PW) was 6.0/5.5 mm = 1.09 in C. aliai and 5.5/7.0 mm = 0.79 in C. stenocephalus ifniensis. In both taxa the prosternal apophysis was elongated, but while its apex was subquadrate in C. stenocephalus ifniensis it was rounded in C. aliai. The elytra were parallel-sided and flattened in C. aliai, ovoid and convex in C. stenocephalus ifniensis. On average, the ratio between length of elytra and maximum width of elytra (EL/EW) was 17.5/11.5 mm = 1.52 in C. aliai and 19.5/13.0 mm = 1.50 in C. stenocephalus ifniensis. In females of both taxa, the apex of the elytra was more acuminate than the one of males. The elytral sculpture was composed by deep striae with coarse punctuation in C. aliai and by slightly marked striae with fine punctuation in C. stenocephalus ifniensis. Legs were proportionally longer in C. aliai than in C. stenocephalus ifniensis.
Both male and female genitalia were found to be very homogeneous within representatives of subgenus Cathoplius. The median lobe of the aedeagus in all taxa was similar either in size or in shape (Figures
Cathoplius species aedeagi. Right lateral aspect of the median lobe (left) and details of its apex (right) in Carabus asperatus from Oualidia (7–8) C. stenocephalus susicus from Aglou (9–10) C. stenocephalus ifniensis from Sidi Ifni (11–12) and C. aliai from Tan-Tan (13–14). Scale bars: 1 mm.
The endophallus in Cathoplius species showed a peculiar morphological feature (Figures
Cathoplius species male and female genitalia. Endophallus of Carabus asperatus from Oualidia, with emphasis on the aggonoporius, saccellus and ostial lobe (15). Details of the saccellar (16) and aggonoporial (17) areas in C. aliai from Tan-Tan. Gonocoxite 2 of the ovipositor in C. asperatus from Oualidia (18) and in C. aliai from Tan-Tan (19). Scale bar: 1 mm.
C. aliai × C. stenocephalus ifniensis hybrids showed intermediate features when compared to parental species. Hybrids were morphologically more similar to the parent female than to the male: hybrid AIF1 (♂ C. aliai × ♀ C. stenocephalus ifniensis) (L 28.0–36.0 mm) was a little more similar to C. stenocephalus ifniensis than hybrid AIF2 (♂ C. stenocephalus ifniensis × ♀ C. aliai) (L 27.0–34.0 mm) which in turn was more similar to C. aliai (Figures
Morphology of pre-imaginal stages. Morphological differences observed among the pre–imaginal stages of the various Cathoplius taxa were corresponding to those reported by
The C. aliai newborn larvae (Figure
Size of Carabus (Cathoplius) aliai Escalera, 1944 and C. (Cathoplius) stenocephalus ifniensis Zarco, 1941 pre–imaginal stages.
Pre–imaginal stages |
C. aliai (length × width, mm) |
C. s. ifniensis (length × width, mm) |
---|---|---|
1st instar larva: | ||
- newborn | 9.5–10.0 × 2.0 | 11.0–11.5 × 2.5 |
- before ecdysis | 15.0–16.5 × 2.5 | 16.5–18.0 × 3.0 |
2nd instar larva: | ||
- after ecdysis | 16.0–16.5 × 3.5 | 17.5–18.0 × 4.0 |
- before ecdysis | 20.0–21.5 × 4.5 | 23.0–24.5 × 5.0 |
3rd instar larva: | ||
- after ecdysis | 21.0–23.0 × 6.0 | 24.0–26.0 × 6.0 |
- before burying | 26.0–30.0 × 6.5 | 28.0–34.0 × 7.0 |
- pre–pupa | 23.0–26.0 × 6.5 | 25.0–29.0 × 7.0 |
Pupa | 20.0–22.0 × 9.0 | 22.0–25.0 × 9.5 |
The aspect of the pupa reflected that of the adult. The C. aliai pupae (Figures
Field observations. The biotope where Carabus (Cathoplius) aliai Escalera, 1944 was found is a sandy and rocky desert area located 15–20 km far from the Atlantic coast, at an elevation comprised between 50 and 200 m a.s.l. (Figure
At the time of the visit to the Tan-Tan northern plateau in 2010, temperatures ranged from 15–17 °C (night) to 19–25 °C (day). Carabus aliai adults and larvae were found from December 17–19 in coincidence with light rains. Adults were seen especially in the late afternoon, coming out from their burrows from underneath the shrubs. Females were preying upon Theba snails while staying hidden into the shrubs. Males were seen running quickly from one shrub to another in search of both snails to eat and females to mate. Burrows consisted in oblique holes about 20 cm deep. Carabus aliai adults were observed while eating mainly T. chudeaui and secondarily T. subdentata meridionalis, but not T. sacchii and E. dillwyniana. Larvae were only seen inside T. subdentata meridionalis shells adhering to L. arborescens branches, at a height from the ground up to 1.5 m. Ecdysis was taking place inside snail shells, where exuviae were normally found. One second instar larva was observed while running on L. arborescens branches, searching for a new snail to prey upon. Predation did not result in snail falling to the ground, instead the shell remained adherent to the shrub branch during the larval meal.
Laboratory observations. After an adaptation period of one–two hours, during which Carabus (Cathoplius) aliai Escalera, 1944 adults were running frenetically in the terrariums, both males and females started digging their own burrows underneath the moss. Burrows were represented by oblique holes with a diameter of 1.5–2 cm reaching the bottom of the terrarium. Adults were hiding inside the burrows during the day and normally came out for feeding and mating in the late afternoon to early morning. Only when barometric pressure was decreasing, did we detect a prolonged running activity throughout the day, especially in males.
Adults of C. aliai, fed with Theba pisana pisana (O.F. Müller, 1774) snails, were very voracious. Due to their elongate head and narrow pronotum they were able to penetrate deep inside the snail’s shell. Each meal lasted for approximately an hour with males and 2–3 hours with females. Males were killing and partially eating an average of 5–6 snails per night. Female meal totals were 1–3 snails per night. Meals were preferably consumed close to the moss side.
Mating occurred during the night and throughout the whole oviposition period. Males were frequently observed on top of females who were feeding. Each mating lasted for approximately an hour. One day after mating, oviposition took place. Females, after digging an oblique gallery in the soil, started laying eggs by inserting their abdomen at a depth and distance between eggs of 1–1.5 cm. Females layed from 1–6 but up to 12–20 eggs per night. When laying was complete, females sealed the gallery. When laid, eggs were diaphanous white in color and measured 4.5 × 1.5 mm. With time, they gradually became light yellow in color. Their size increased during embryonic development, reaching 5.0 × 2.0 mm. The embryonic development was completed in 15 days. Under laboratory conditions, the duration of the oviposition period in C. aliai was 100–110 days, from December to March. During this time, the four females laid 277, 282, 298 and 307 eggs, respectively. Two oviposition periods, separated by a short pause (10 days) in January, were noticed. On average, the total productivity of C. aliai in 95 laying days was 291 eggs/female, with a laying frequency of 3 eggs/night. Following reproduction, all C. aliai breeders died without undergoing summer diapause.
In contrast to C. aliai, the reproduction cycle of C. (Cathoplius) stenocephalus ifniensis Zarco, 1941 consisted in a first winter and a second spring oviposition cycle, separated from each other by a short burial period (30 days). When the spring cycle ended, breeders buried again and fell into a long summer diapause that lasted until the following winter time, when a scarce number of eggs and viable larvae was produced before breeders died. The average total productivity of C. stenocephalus ifniensis in 120 laying days was 338 eggs/female (laying frequency of 2.8 eggs/night), subdivided in 242 eggs laid in 75 days during the first oviposition cycle (3.2 eggs/night) and 96 eggs laid in 45 days during the second cycle (2.1 eggs/night).
After hatching, C. aliai larvae remained in the egg cell for a day to complete sclerification. Once on the surface, newborn larvae begun running around the terrarium searching for snails to feed on. When snails were found, larvae penetrated the shell by keeping their ventral side of the body adhering to the shell walls. Despite their small size [10.0 × 2.0 mm (length × width)], C. aliai first instar larvae were found to be very aggressive, being able to kill also large T. pisana pisana snails. For the completion of the first instar period, two meals (each lasting 1.5 days) with snails of small size (shell width 10 mm) were necessary. The pre-ecdysis period and ecdysis lasted 2 days. Ecdysis always took place inside snail shells. Exuviae were then found inside the shells.
The C. aliai second instar larvae (16.0 × 3.5 mm in size) began feeding after integument sclerification, which stood one day. For the completion of the second instar period, three meals (each lasting 1.5 days) with snails of intermediate size (shell width 15 mm) were necessary. The pre-ecdysis period and ecdysis lasted 2.5 days. Ecdysis generally took place inside snail shells or in a pit dug under the shelter or into the soil.
After integument sclerification of one day, the third instar larvae (22.0 × 6.0 mm in size) began feeding again. For the completion of the third instar period, four meals (each lasting 2 days) with snails of large size (shell width 20 mm) were necessary. Then, the mature larvae (28.0 × 6.5 mm in size) stopped feeding and started digging a large cell in the soil for pupating. Inside the pupal cell, pre-pupas (24.0 × 6.5 mm in size) and pupas (21.0 × 9.0 mm in size) occupied 2/3 of the cell length. After emergence from the pupa, C. aliai neo-adults remained in the pupal cell for about 3 days before rising to the surface.
Under laboratory conditions, the duration of the development cycle from egg fertilization to the rising of neo-adult averaged 2 days shorter in C. aliai compared to C. stenocephalus ifniensis (70 vs. 72 days). While embryonic development lasted 15 days in both species, larval development on the surface (from egg hatching to digging of the pupal cell), as well as the burial phase, were one day shorter in C. aliai than in C. stenocephalus ifniensis (23 vs. 24 and 32 vs. 33 days, respectively). More specifically, the duration of the first instar period (6 vs. 7 days), the duration of the prepupal period (8 vs. 9 days) and the time between emergence from the pupa and the rising to the surface of neo-adults (3 vs. 5 days) were a little shorter in C. aliai than in C. stenocephalus ifniensis, while the duration of the pupal instar was a little longer (21 vs. 19 days) (Table
Differences between Carabus (Cathoplius) aliai Escalera, 1944 and C. (Cathoplius) stenocephalus ifniensis Zarco, 1941 life cycles at the same laboratory conditions [temperature 15/19–17/21 °C (night/day); photoperiod 9–13 hours of daylight].
Life cycle phases | C. aliai (mean days) | C. s. ifniensis (mean days) |
---|---|---|
Embryonic development: | 15 | 15 |
- mating – oviposition | 1 | 1 |
- oviposition – hatching of larvae | 14 | 14 |
Larval development on the surface: | 23 | 24 |
- 1st larval instar | 6 | 7 |
- 2nd larval instar | 8 | 8 |
- 3rd larval instar | 9 | 9 |
Burial phase: | 32 | 33 |
- pre–pupa | 8 | 9 |
- pupa | 21 | 19 |
- adult emergence – rising to the surface | 3 | 5 |
Duration of development cycle | 70 | 72 |
Completion of adult sclerification | 21 | 21 |
Time from hardening to burying | 2 | 15 |
Burial phase (gonad maturation) | – | 30 |
Spring oviposition cycle | – | 50 or 0 |
Burial phase (summer diapause) | 250 | 180 or 220 |
Winter oviposition cycle | 95 | 75 |
End of oviposition – death | 15 | 15 |
Life span (larva + pupa + adult) | 453 | 458 |
Under laboratory conditions, the rising to the surface of C. aliai neo-adults took place from the beginning of February through mid-April. The mean survival rate from egg to adult was 53% and the final ratio between males and females was of 1:1. Males rose to the surface a little earlier than females. Once on the surface, neo-adults fed on T. pisana pisana snails until their total hardening, which was completed in approximately 3 weeks. During this period, neo-adults were very aggressive, killing a large number of snails throughout the day. Both males and females were partially eating an average of 9–10 snails per day. Even with optimal temperature and humidity conditions, a few days after completing sclerification neo-adults buried themselves and fell into a long summer diapause (8–9 months, starting from April–May) without reproducing. Adults rose to the surface again at the end of November, commencing their oviposition cycle that lasted for 3.5 months until mid-March. Egg production averaged 250 eggs/female. Following reproduction, adults died. Females died a few days after discontinuing oviposition. Males survived approximately 2 weeks longer than females. No feeding attempts were observed during this period. The average life span of C. aliai under laboratory conditions was 15 months (including 2 months as pre-imaginal stages) (Table
In C. stenocephalus ifniensis the pattern was found to be similar (the mean survival rate from egg to adult was 52% and the final ratio between males and females was of 1:1), but the reproduction cycle was different. Neo-adults of this taxon, after rising to the surface and completing sclerification in approximately 3 weeks, remained on the surface for about two weeks and then underwent a burial phase that lasted for a month. During this phase, gonad maturation was taking place. By mid-March, precocious neo-adults rose to the surface and started reproducing, but their cycle was short (1.5 months) and egg production was scarce (average of 100 eggs/female). Only one third of neo-adults took part in the spring oviposition cycle, while the majority of individuals remained buried without reproducing. At the end of April–beginning of May, adults that reproduced buried themselves and fell into diapause for 6 months. At mid-November, all individuals rose to the surface and started reproducing. The winter oviposition cycle lasted for 2.5 months and egg production was high (average of 250 eggs/female). Following reproduction, adults died. When considering the two oviposition cycles, the average egg production in C. stenocephalus ifniensis was 350 eggs/female (100 eggs/female more than in C. aliai). The average life span of C. stenocephalus ifniensis under laboratory conditions was 15 months (Table
Hybrids behavior. Hybridization between Carabus (Cathoplius) aliai Escalera, 1944 and C. (Cathoplius) stenocephalus ifniensis Zarco, 1941 led to the following results:
1) C. aliai ♂ × C. stenocephalus ifniensis ♀ crossbreeding (AIF1). Mating occurred normally, but in a less intensive manner than in pure C. aliai and C. stenocephalus ifniensis breeding. Oviposition took place a day after copulation. Females layed from 1 to 4 eggs per night. The average total productivity was 87 eggs/female over a period of 65 days. Following reproduction, adults buried themselves and fell into diapause. Besides a reduced oviposition rate compared to the normal one of the parental taxa, hybridization resulted in a reduced hatching rate and an increased pre-imaginal mortality rate that led to a F1 mean survival rate from egg to adult of 33%, versus 53% in C. aliai and 52% in C. stenocephalus ifniensis. The duration of the development cycle in hybrid AIF1 was 74 days, subdivided into 15 days for embryonic development, 25 days for larval development on the surface and 34 days for the burial phase. Sclerification of neo-adults was completed in about 3 weeks. Afterwards, neo-adults remained on the surface for 3–4 weeks before falling into diapause. Hybrids had a sturdiness similar to that of pure C. aliai or C. stenocephalus ifniensis specimens, with a life span of 12–15 months.
The F1 crossbreeding (AIF1 × AIF1) led to a reduced fecundity rate (41 eggs/female over a period of 45 days), to neonatal mortality with scarcely viable F2 pre-imaginal stages (70% mortality rate for first instar larvae, 48% for second instar larvae, 32% for third instar larvae, 80% for pre-pupas and pupas) and to stillbirth with non-viable F2 imagoes (100% mortality rate inside the pupal cell, without any rising to the surface of neo-adults).
2) C. stenocephalus ifniensis ♂ × C. aliai ♀ crossbreeding (AIF2). The behavior was found to be similar to that seen in the previous combination. The average total productivity was 69 eggs/female over a period of 75 days. Two oviposition periods, separated by a short pause (15 days), were noticed. Also in this case, hybridization was responsible for a reduced hatching rate and an increased pre-imaginal mortality rate that led to a F1 mean survival rate from egg to adult of 31%. The duration of the development cycle in hybrid AIF2 was 72 days, subdivided into 15 days for embryonic development, 24 days for larval development on the surface and 33 days for the burial phase. After sclerification, neo-adults remained on the surface for about 2 weeks before falling into diapause.
The F1 crossbreeding (AIF2 × AIF2) led to a reduced fecundity rate (33 eggs/female over a period of 53 days), to neonatal mortality with scarcely viable F2 pre-imaginal stages (82% mortality rate for first instar larvae, 50% for second instar larvae, 34% for third instar larvae, 84% for pre-pupas and pupas) and to stillbirth with non-viable F2 imagoes (100% mortality rate inside the pupal cell).
Morphology. The subgenus Cathoplius within the Genus Carabus includes ground beetles characterized by strongly sclerified integument, black in color, brachypterous, with elytra that are joined along the suture, an achetous, ellipsoidal, silphoid or cychrized pronotum, and a narrow and very elongate head (
The morphological differences between C. aliai and C. stenocephalus (sensu lato) are remarkable. The pronotum profile and the elytral sculpture are very peculiar. Despite their close range of distribution (only 50 km are dividing Sidi Ifni Beach from Plage Blanche), differences are striking when C. aliai adults are compared to those of C. stenocephalus ifniensis Zarco, 1941. These differences include a smaller size, a much slender silhouette, a more brilliant aspect, longer legs, and a wider and a little more curved apex of the median lobe of the aedeagus. Differences are also present referring to pre-imaginal stages: C. aliai larvae are much smaller than those of C. stenocephalus ifniensis (9.5 × 2.0 mm vs. 11.0 × 2.5 mm in newborn larvae) and the C. aliai pupa is also smaller, with a narrower thoracic area and a different chaetotaxy. Both imaginal and pre-imaginal features are an index of the specific differentiation between the two taxa.
Life cycle. The 2010 raining season in the Tan-Tan area began on November 30, with a storm (17 mm of rain at a temperature of 16–23 °C) that induced the rising of Carabus (Cathoplius) aliai Escalera, 1944 adults from their summer diapause. Oviposition occurred some days later, with eggs hatching on December 13–14 and first ecdysis on December 18–19, when second instar larvae were found. The second ecdysis occurred at the laboratory on December 28–31 and the burying of third instar larvae on January 7–9, with rising to the surface of neo-adults on February 8–15. Out of the ten wild larvae found, two died as second instar and two as third instar, and out of the six surviving adults, four were males and two were females. The 60% survival rate noticed for wild larvae matches the mean survival rate of 53% obtained at the laboratory from egg to adult, but the ratio between males and females does not (2:1 in nature vs. 1:1 at the laboratory). This is probably due to the fact that, after emergence, precocious males are rising to the surface earlier than first females.
In mid-March C. aliai neo-adults buried themselves and fell into a summer diapause that lasted until late autumn, when terrariums were abundantly watered. When watering was carried out during late spring or in summer, adults were rising to the surface, feeding for some days and burying again without mating. The beginning of reproduction in representatives of subgenus Cathoplius depends exclusively on the start of the natural raining season (
While under laboratory conditions the oviposition period in C. aliai lasted for over three months, in nature this is not the normal case. Aridity and cold weather at night are responsible for a lack of active Theba snails, and correspondingly no activity of C. aliai adults and larvae is present in January in the Tan-Tan area. In nature, the oviposition period probably lasts for a month, from the beginning to the end of December, and after reproduction all adults die. The C. aliai life cycle can therefore be placed into the winter breeders with short larval development type sensu
One of the most striking features in representatives of the subgenus Cathoplius is their high fecundity rate. Species belonging to this subgenus are one of the most prolific among the known ground beetles (
The mean duration of the development cycle, from egg fertilization to the rising of neo-adults, was found to be shorter in C. aliai than in C. stenocephalus ifniensis. Results of the present study are in agreement with those obtained by
From the behavioral point of view, C. aliai is a typical sabulicolous steppe wandering species (
In the field, C. aliai adults were observed mainly feeding upon T. chudeaui (Germain, 1908) and secondarily upon T. subdentata meridionalis snails. This is likely due to the major shell width, the larger aperture and the lack of a parietal denticle in T. chudeaui. The fact that Eremina dillwyniana (Pfeiffer, 1851) snails, which are abundant in the Tan-Tan area, were not eaten by C. aliai is an additional proof that representatives of subgenus Cathoplius feed exclusively on Theba snails. First and second instar C. aliai larvae were only found inside T. subdentata meridionalis shells adhering to Launaea arborescens branches. The completion of the first pre-imaginal stage on vegetation is probably essential for C. aliai larval survival, in order to avoid predation from associated carabids. At the Tan-Tan biotope several very aggressive species are present, such as Anthia (Termophilum) sexmaculata (Fabricius, 1787), Scarites (Scallophorites) buparius (Forster, 1771) and Sphodrus leucophthalmus (Linnaeus, 1758) (Ghittino, personal observations). T. subdentata meridionalis snails are probably the prey of choice for C. aliai larvae for their minor shell width, the smaller aperture and the presence of a well developed parietal denticle that better protects larvae from aggressions.
As predators of live Theba snails, Cathoplius should play an important role in the ecosystem by reducing Theba proliferation which can be detrimental to both conservation of the scarce vegetation in arid areas and to animal husbandry, by preventing important livestock parasitic diseases among grazing land animals (
We could not find any reports of Theba subdentata meridionalis or T. chudeaui acting as intermediate hosts for sheep and goat lungworms but the presence of the pathology in animals and the observation of worm stages in snails are evidence of their involvement in the disease life cycle. Differently from other local snails, T. subdentata meridionalis and T. chudeaui live on shrubs that are particularly appreciated by sheep and goats (e.g. Launaea arborescens and Lycium intricatum) which then can be easily infected through accidental ingestion of parasitized snails.
Under laboratory conditions, C. aliai adults and larvae were found to be very aggressive against Theba snails. Adults killed up to 5–6 snails per night over a period of three months. For completing the development cycle, each larva fed on an average of nine snails and to reach complete sclerification neo-adults killed up to 9–10 snails per day over a period of three weeks. These data indicate that C. aliai is an efficacious natural enemy of Theba snails that can also reduce the impact of some economically important ruminant diseases. Conservation of C. aliai in southern Morocco is therefore recommended.
Hybridization. The results of our hybridization experiments between Carabus (Cathoplius) aliai Escalera, 1944 and C. (Cathoplius) stenocephalus ifniensis Zarco, 1941 are in agreement with those obtained by
The F1 hybrids crossbreeding (AIF1♂ × AIF1♀ and AIF2♂ × AIF2♀) led to a further reduction of laid eggs and a very high mortality rate during embryonic, larval and pupal development. This was also more evident in the AIF2 than in the AIF1 combination. Only a few F2 immature imagoes were obtained (3 out of 120 larvae for AIF1 and 1 out of 100 larvae for AIF2), but these specimens died in the pupal cell within 10 days from emergence. Since no vital neo-adults were available, it was impossible to carry out subsequent F2 hybrids crossbreeding.
Through our crossbreeding experiments, that employed a high number of F1 hybrids (4 mating pairs for each combination) maintained at natural conditions with regards to temperature and photoperiod, we demonstrated that a marked reproductive isolation between C. aliai and C. stenocephalus is present. This isolation corroborates the distinction at a species level of the two taxa and is similar to the isolation observed between C. stenocephalus and C. asperatus (
Data generated in this study, together with those obtained by
According to these results, three Cathoplius species are spread along the Moroccan Atlantic coast: C. (Cathoplius) asperatus (Dejean, 1826) in the north, C. stenocephalus Lucas, 1866 in the center and C. aliai Escalera, 1944 in the south (Figure
A distributional gap, probably due to the lack of ad hoc investigations, is actually present between northern and southern C. aliai populations. Northern populations dwell in Guelmim (Plage Blanche) and Tan-Tan (Ben Khlil, Tan-Tan, Abteh) provinces, while southern populations are spread from present Laâyoune (Izik plateau, Sabkhat Tislatine, Bou Kra) to Boujdour (Lemsid, Metmarfag) provinces. The 200 km area in between, corresponding to present Tarfaya province, is represented by a very sandy desert with a few spots suitable for C. aliai such those around Akhfennir, Daoura and El Hagounia. Searches of this area during the favorable season will probably allow the identification of new C. aliai populations.
This work is dedicated to the memory of Dr Joaquin Mateu (Barcelona, 9/1/1921–18/1/2015), who really discovered and first studied C. aliai. The authors are grateful to Dr Thierry Deuve (Muséum National d’Histoire Naturelle, Paris) for some important advices. A particular thank is also due to Mr Jaroslav Kaláb (Kuřim, Czechia) and to Dr Massimo Meregalli (Department of Animal and Human Biology, University of Turin, Italy) for information on habitats and photos, and to Prof. Ronald Hedrick (School of Veterinary Medicine, University of California, Davis, CA, USA) for his assistance in editing the English text of the manuscript.